Do mosquitoes influence bat activity in coastal habitats

LeroyGonsalvesAD Susan LambA CameronWebbB Bradley LawC and VaughanMonamyA

ASchoolofArts andSciencesAustralianCatholicUniversity 40EdwardStreetNorthSydneyNSW2060AustraliaBDepartment of Medical Entomology Westmead Hospital and University of Sydney Westmead NSW 2145Australia

CForest Science Centre Department of Primary Industries PO Box 100 Beecroft NSW 2119 AustraliaDCorresponding author Email leroygonsalvesacueduau

AbstractContext Conservation of insectivorous bat populations requires appropriate management of foraging habitats and the

prey resources they sustain Endangered coastal saltmarsh communities support a diverse range of aquatic and terrestrialarthropods including the saltmarsh mosquito (Aedes vigilax Skuse) an important vector of mosquito-borne viruses and apotentially important prey resource for insectivorous bats Prey detectability by bats is considered to be limited with low-frequency echolocation particularly in cluttered habitats that may render abundant Ae vigilax populations unavailable tosome bat species

AimsTo investigate relationships between availability ofAe vigilax and non-mosquito prey and the activity of foraginginsectivorous bats in a range of coastal habitats

MethodsWemeasured nightly bat activity and the abundance of prey (mosquito and non-mosquito) concurrently duringneap and spring tides in saltmarsh urban and forest habitats Comparisons were made between tidal cycle and habitats andrelationships between bat activity and the abundance of prey were examined

Key resultsWhereas prey abundanceswere generally greatest in saltmarsh and forest habitats bat activitywas greatest inthe forest habitatHowever proportional feeding activitywasgreatest in saltmarsh Prey abundancewas positively correlatedwith total bat activity only in the open saltmarsh where an absence of clutter would maximise prey detectability and thusavailability Positive correlations betweenAe vigilax abundance and bat activity across all habitats were restricted to bats ofthe Vespadelus genus which are small-sized bats that employ high-frequency echolocation suitable for detection of smallprey along edges

Conclusions These findings suggest that Ae vigilax may be an important prey resource for small high-frequencyecholocating bats capable of discerning small prey within cluttered forest as well as exploiting abundant prey in the opensaltmarsh

Implications Small high-frequency echolocating bats should be the focus of future studies investigating the importanceof small prey such as Ae vigilax to the diets of foraging bats

Received 16 August 2012 accepted 10 December 2012 published online 30 January 2013

Introduction

The conservation of insectivorous bat fauna requires anunderstanding of species-specific biology and ecology Animportant requirement is a detailed understanding of theassociations between bats and their foraging habitats (Fenton1997) Given bats can be highly mobile (Law and Lean 1999Cryan et al 2000 OrsquoDonnell 2001) they may be able to accessa diverse range of habitats (Fenton 1997) However not allhabitats sustain similar bat assemblages

Patterns of bat activity have been documented for a widerange of habitats including riparian forests (Lloyd et al 2006)temperate forests (OrsquoDonnell 2000) agricultural paddocks(Gehrt and Chelsvig 2003 Wickramasinghe et al 2003Lumsden and Bennett 2005) deserts (Fenton and Morris 1976Bell 1980 Kuenzi and Morrison 2003) wetlands (Menzel et al2005 Lookingbill et al 2010) and urban areas (Avila-Flores

and Fenton 2005 Hourigan et al 2006 Threlfall et al 2011)Only recently has use of coastal saltmarsh by insectivorous batsbeen documented (Hoye 2002 Laegdsgaard et al 2004 Belbaseacute2005 Lamb 2009 Gonsalves et al in press) The use of thisproductive but endangered and declining ecological community(Saintilan and Williams 1999) by several threatened bat specieshighlights the need for further investigation of bats using thishabitat

Coastal saltmarsh represents suitable breeding habitat forseveral estuarine mosquito species The saltmarsh mosquito(Aedes vigilax Skuse) can be locally abundant throughoutsummer (Webb and Russell 2009) representing a potentiallyimportant prey resource for insectivorous bats foragingwithin coastal saltmarsh habitats However Ae vigilax hasbeen identified as an important vector of mosquito-borneviruses such as Ross River virus and Barmah Forest virus

CSIRO PUBLISHING

Wildlife Research 2013 40 10ndash24httpdxdoiorg101071WR12148

Journal compilation CSIRO 2013 wwwpublishcsiroaujournalswr

Notwithstanding the health risks associated with Ae vigilax themosquito also generates nuisance biting impacts In response tothe health and social impacts ofAe vigilax broad-scale mosquitocontrol has been implemented in many coastal areas (Bell 1989Russell and Kay 2008) with Bacillus thuringiensis israelensis(Bti) the most commonly used microbial larvicide used in thereduction of larval mosquito populations (Russell and Kay 2008Poulin et al 2010) Concern has been raised as to the potentialimpact that broad-scale mosquito-control activities may have onlocal bat species (Laegdsgaard et al 2004) however althoughthere is evidence that mosquitoes may be an important dietaryitem for insectivorousbats foragingwithin saltmarsh (Hoye2002Laegdsgaard et al 2004Belbaseacute 2005 Lamb2009) no studyhasspecifically investigated relationships between the abundance ofAe vigilax and bat activity

Although the immature aquatic stageofAe vigilax is generallylimited to estuarine habitats the adults can disperse widely withbiting impacts being experienced at a distance of over 5 km fromestuarine habitats (Webb and Russell 2009) Forested habitatsare considered refuge habitats that provide sheltered areas formosquitoes while also supporting sources of blood meals thatfemale Ae vigilax individuals require for egg developmentConsequently any investigation of relationships betweenbat activity and Ae vigilax abundance should also seek toinvestigate other habitats to which Ae vigilax may disperse onemergence from coastal saltmarsh habitat

Along the eastern Australian coast large areas of saltmarshhabitat can produce abundant Ae vigilax populations andadjacent forest and woodland habitats may provide suitablerefuge habitat for adult mosquitoes (Webb and Russell 2009)These habitats also are known to sustain hollow- and cave-roosting insectivorous bat species (Payne 2006) Locatedbetween the larval habitat and potential refuge habitat ofAe vigilax lies built-up urban habitat that may also providesuitable larval habitat for many container-breeding mosquitoesand also refuge habitat for othermosquitoes aswell asAe vigilaxAn investigation of the patterns of Ae vigilax abundance andbat activity in these three habitat types may elucidate anyrelationships between Ae vigilax abundance and bat activity

Foraging activity of bats can be influenced by several factorsPrey abundance has been found to influence activity of bats indifferent habitat types (Rydell 1989 Fenton 1990 Rautenbachet al 1996 Fukui et al 2006 Adams et al 2009) as hasvegetation clutter (ie structures that produce non-targetechoes) (OrsquoNeill and Taylor 1986 Bradshaw 1996 Brighamet al 1997 Law and Chidel 2002 Lloyd et al 2006) Vegetationclutter can also influence bat mobility so that bats with aparticular wing morphology and echolocation design displaydifferential habitat use (Neuweiler 1984 Norberg and Rayner1987 Fenton 1990 Saunders and Barclay 1992 Brigham et al1997) Fast-flying bats that are less manoeuvrable generallyhave a high wing aspect ratio (Rhodes 2002) with low-frequency echolocation calls that make it difficult to navigateor detect prey in high levels of clutter (Moslashhl 1988 Barclay andBrigham 1991) These clutter-sensitive bats have been groupedtogether to form an open-space foraging guild (Schnitzler andKalko 2001 Adams et al 2009) The sensitivity to clutter ofthis guild of bats would suggest that they would use more openareas for foraging

Although prey abundance and vegetation clutter on theirown are known to influence the habitats in which bats foragethe effects of these two factors are also known to interact witheach other such that prey abundance does not necessarilyequate to its availability to bats (Boonman et al 1998 Adamset al 2009Rainho et al 2010) Furthermore it is unclearwhetherecholocation design particularly echolocation frequency limitsthe size of prey that can be located by foraging bats Longerwavelengths associated with low-frequency echolocation arethought to be unsuited to detection of small prey at distancessufficient for interception by bats (Barclay and Brigham 1991)Since bat size is negatively correlated with echolocationfrequency (Jones 1999) larger (less-manoeuvrable) bats arethought to be restricted to larger prey whereas smaller batsable to detect large prey are restricted to smaller prey becauseof morphological constraints (eg prey hardness and jaw size ndashFreeman andLemen 2007) Howevermany studies investigatingdiets of mediumndashlarge-size bats have reported the presenceof many small dipterans (chironomids and mosquitoes)Waters et al (1995) challenged the assumption that smallprey are unavailable to large bats that employ low-frequencyecholocation and proposed that detection ranges of prey size aregenerally independent of echolocation frequency

If Ae vigilax is an important prey resource for insectivorousbats one would predict relationships between bat activity andAe vigilax abundance to be positively associated with thestrength of this association dependent on the importance ofAe vigilax to the diets of individual species However givenlimitations imposed on foraging bats by vegetation clutter aswell as the restrictions in prey size associated with particularecholocation designs it is unclear whether relationships betweenAe vigilax abundance and bat activity as well as activity ofindividual species are consistent across habitats with varyinglevels of clutter To elucidate relationships between Ae vigilaxabundance and bat activity that may be inconsistent amonghabitats or bat species we surveyed bat activity and activity ofindividual species as well as prey (Ae vigilax and non-mosquito)abundance in saltmarsh urban and forest habitats which varybroadly in acoustic complexity (least-to-greatest) We predictthat (1) relationships between Ae vigilax abundance and batactivity (including feeding) will not be consistent across habitatsor species (2) stronger associations between prey (Ae vigilaxand non-mosquito) abundancewill occur in less cluttered habitats(saltmarsh) although not restricted to these particularlyfor small-sized bats that employ high-frequency echolocationand (3) positive associations will occur between Ae vigilaxabundance and those species that utilise Ae vigilax as a preyresource whereas the activity of other bat species will becorrelated with the abundance of non-mosquito prey

Materials and methodsStudy site

The study areawas located in theEmpireBay region (332905700S1512104000E)of theCentralCoast ofNewSouthWalesAustralia(Fig 1) This region is ~50 km north of Sydney and experiencesa warm subtropical climate

The study area is characterised by more than 40 vegetationcommunities many of which occur within a large national park

Do mosquitoes influence bat activity Wildlife Research 11

(Bouddi National Park 1189 ha) and five smaller nature reserves(Cockle Bay Nature Reserve 685 ha Rileys Island NatureReserve 457 ha Pelican Island Nature Reserve 40 haSaratoga Island Nature Reserve 2 ha) The national park andnature reserves support populations of hollow- and cave-roosting insectivorous bats including six threatened specieslisted under the NSW Threatened Species Conservation Act1995 (Payne 2006) Coastal saltmarsh urban areas and forestsrepresent three major habitats in the study area These habitatsare grossly different from one another and characteristics ofeach of these habitats are described below

Coastal saltmarsh habitat is characterised by low-growingsalt-tolerant succulent herbs such as samphire (Sarcocorniaquinqueflora (Bunge ex Ung-Sternb) AJScott) and creepingbrookweed (Samolus repens (JRForst amp GForst) Pers)Although saltmarsh lacks trees a small number of greymangrove shrubs (Avicennia marina (Forsk) Vierh) (lt3mhigh) occurred in patches as a result of the landwardtransgression of mangroves (Saintilan and Williams 1999)This vegetation community represents important larval habitatsfor many estuarine mosquito species including Ae vigilaxHexham grey (Ae alternans Westwood) and saltmarshculex (Culex sitiens Wiedemann) (Webb and Russell 2009)Additionally coastal saltmarsh communities have been foundto supportmoderately high levels of bat activity (Lamb2009) andrepresent important foraging habitats for bats (Belbaseacute 2005)

Urban habitat is characterised primarily by residential areasthat include dwellings and structures associated with residential

areas such as schools roads and street lights Urban habitatsprovide a range of suitable larval habitats for urban mosquitospecies such as domestic container mosquito (Ae notoscriptusSkuse) brown house mosquito (Cx quiquefasciatus Say) andundergroundmosquito (CxmolestusForskal) (Webb andRussell2009) Urban areas also sustain a diverse range of bat species andtypically support lower levels of bat activity (Avila-Flores andFenton 2005 Scanlon and Petit 2008 Hourigan et al 2010Threlfall et al 2011 2012) However species diversity andactivity levels within urban habitats vary with the degree ofurbanisation (Hourigan et al 2006 Threlfall et al 20112012) Although no attempt has been made to define the urbanhabitat on the basis of the degree of urbanisation residentialdensity in the overall study area was relatively low (25 dwellingshandash1) and could be classified as suburban The close proximity ofurban areas to saltmarsh and forest habitats meant that withinthe urban habitat patches of moderately vegetated areas werepresent Although attempts were made to avoid sampling nearthese patches thiswas not always possible given the small extentof urban spacewithin the study area aswell as limitations imposedby landowners All sampling was undertaken in a mannerthat attempted to minimise the influence of these vegetatedareas (ie detectors were oriented away from vegetation andarthropod sampling was conducted at the furthest practicallypossible distance away fromvegetation being ~30ndash420maway)

The forest habitat is situated on an escarpment thatstraddles the landward side of the urban habitat Sampling ofthis habitat was undertaken in Narrabeen Coastal Blackbutt

Saltmarsh

Urban

Forest

Block 0 05 1 Kilometers

Fig 1 Satellite image of study area (adapted from Google Earth) Sampling location star = saltmarsh triangle = urbandoughnut = forest in each blocked site

12 Wildlife Research L Gonsalves et al

Forest within Bouddi National Park Dominated by blackbutt(Eucalyptus pilularis Smith) turpentine (Syncarpia glomuliferasubsp glomulifera Smith) and bakers oak (Allocasuarinatorulosa (Aiton) LASJohnson) this vegetation communityhas a typical canopy height of 20m occurring on Narrabeensandstone that supports a sparse-to-moderate understoreyof shrubs and a well developed grass layer (Bell 2009) With~40 canopy cover this vegetation community can be describedas an open forest (Specht 1970) The forest habitat containsareas that provide suitable larval habitats for many floodwaterspecies including Ae multiplex Theobald Ae procax Skuseand brackish forest mosquito (Verrallina funerea Theobald)Additionally forest communities are known to sustain severalhollow- and cave-roosting bats (Payne 2006) and represent animportant habitat for foraging bats in the study area (Lamb 2009)

Study design

We surveyed insectivorous bat activity and the abundancesof mosquito fauna and other volant insect fauna at four sites(Empire Bay Cockle Bay Palmers Lane and Bensville) withinthe study area Each site was considered a block containingcorresponding saltmarsh urban and forest habitats that weresampled concurrently (Fig 1) Sites were surveyed from duskto dawn over three consecutive nights each fortnight fromDecember 2008 to April 2009 All sampling was carried out ata consistent point within each site (ie sampling sites were notshiftedwithin each site after each sampling occasion) The start ofeach fortnight coincided with a spring or a neap tide which isconsidered to have a strong influence on Ae vigilax abundance(de Little et al 2009 Kokkinn et al 2009) Data were collectedover five spring tides and four neap tides with two sites surveyedconcurrently each fortnight

Bat survey

In each habitat one Anabat SD1 detector (Titley ElectronicsBallina NSW Australia) was set at a height of 1m and at a 45

angle to the ground facing open areas (interior of saltmarshaway from structures in urban areas and along fire trails withinforested areas) Detectors recorded navigational and feedingecholocation calls of microchiropteran bats that vary fromspecies to species and can be used to differentiate among mostspeciesAll recordingswere stored on a compactflash card beforebeing uploaded to a laptop for analysis Recorded bat calls wereidentified to species where possible using the automated call-identification software AnaScheme (Gibson and Lumsden2003) in association with a key for the lower north-easternNew South Wales coastal plain (Adams et al 2010) Testingof this key revealed that 05 of all calls (n= 191) wereincorrectly identified with misidentifications restricted to callsfrom a single species (large forest bat Vespadelus darlingtoniAllen) (Adams et al 2010) Bat calls with fewer than three validpulses (ie minimum of six data points and model quality of09) were not analysed by AnaScheme Because multiple batspecies may call simultaneously calls were assigned to a speciesonly if gt50of pulses within the sequencewere attributed to thatspecies and only passeswith aminimumof three pulses classifiedto the same species were identified All calls that could not be

assigned to a bat taxonwere included in counts of total bat activitybut were labelled as lsquounidentifiedrsquo

Echolocation calls of certain species overlap to such adegree that it is not possible to differentiate among themConsequently the identification key grouped certain speciestogether (eg Gouldrsquos long-eared bat Nyctophilus gouldiTomes and lesser long-eared bat N geoffroyi Leach =Nyctophilus spp eastern forest bat V pumilus Gray easterncave bat V troughtoni Kitchener Jones amp Caputi and littleforest bat V vulturnus Thomas =Vespadelus spp) AlthoughV troughtoni calls could contribute to the activity of theVespadelus species group intensive harp trapping in the area(throughout a field season) failed to catch any V troughtoniindividuals suggesting that the activity of Vespadelus spp islikely to represent the activity of V pumilus and V vulturnusonly both of which were commonly captured in harp traps(Gonsalves 2012) All identified calls were screened manuallyfor feeding buzzes ndash a rapid increase in pulse-repetition rateslope frequencyand speed (associatedwithpursuit and captureofprey Griffin et al 1960 Pennay et al 2004) For each detectorand each night the number of bat passes and number of feedingbuzzes for each species was tabulated

Prey survey

In each habitat mosquito abundance was surveyed nightly withtwo CO2-baited encephalitis-virus surveillance (EVS) traps(Rohe and Fall 1979) (Australian Entomological SuppliesBangalow NSW Australia) whereas other aerial insect faunawere sampled with one light trap (Australian EntomologicalSupplies Bangalow NSW Australia) All traps were set at aminimumdistance of 10m frombat detectors Trapswere set nearstructures (isolated mangroves within coastal saltmarsh gardenshrubs in urban areas and vegetation along the edge of a fire trailin forested areas) in each habitat that allowed EVS traps to besuspended Mosquito collections were identified to speciesaccording to keys (Russell 1996) and the abundance of eachspecies was recorded All light-trap specimens were sorted intothree insect orders (Lepidoptera Coleoptera Diptera) with anyother specimens pooled into an lsquootherrsquo category These insectgroups were then further sorted by size into four size classes(tip of head to tip of abdomen) (lt5mm 5ndash9mm 10ndash14mm andgt14mm) Counts of all insects thenwere carried out and recordedfor each night of trapping in each habitat Insects were oven-driedat 60C for a minimum of 48 h until a constant weight could berecorded (to nearest 1 105 g) For samples withmore than 100insects in a lt5-mm size class the mass of the total sample wasused along with regression equations (calculated for each taxonby using count and dry-weight data obtained for all other samplesof insects lt5mm) to estimate the abundance of the sample

Data analyses

Prior to analysis all collected data were log-transformed andaveraged across consecutive nights for each site during eachfortnight Although dry-weight data were available for all insecttaxa and size classes only abundance values were used inanalyses to allow for comparison with Ae vigilax for whichonly abundance values were available A repeated-measuresmixed-model ANOVA was used to test for effects of habitat

Do mosquitoes influence bat activity Wildlife Research 13

(saltmarshurbanforest) tidal cycle (neapspring) and allinteractions on mean nightly bat activity the activity of thecommonly recorded species (representing gt050 of total batactivity) Ae vigilax abundance and the abundance of othervolant insects An autoregressive order-one covariancestructure was used for the repeated factor (tidal cycle) in eachanalysis because this covariance structure assumes thatmeasurements taken close to one another in time will be moreclosely correlated than measurements taken at greater intervalsin time Comparisons of main effects were Bonferroni correctedfor multiple comparisons For each dependent variable if datawere not normally distributed a KruskalndashWallis test was insteadused to examine the effect of each independent variable

A goodness of fit chi-square test was used to compareproportional feeding activity (proportion of bat callscontaining feeding buzzes) and the proportional feedingactivity of individual species between habitats and tidal cyclewhereas best-subsets regression analysis was used to examinerelationships among the abundances of non-mosquito prey(lepidopterans coleopterans dipterans other insects all taxapooled insects lt5mm insects 5ndash9mm insects 10ndash14mm andinsects gt14mm) Ae vigilax abundance and bat activity aswell as the activity of the commonly recorded bat species(representing gt050 of total bat activity) No climaticvariables (eg temperature humidity wind) were incorporatedinto regression models Selection of models for each dependentvariable was based on Akaike information criteria scorescorrected for small sample sizes (AICc) Since vegetationclutter influences prey detectability (Adams et al 2009Rainho et al 2010) analyses were conducted for each habitatseparately Given insect abundances vary with height withinforests (Adams et al 2009) it was considered that preytrapped in light traps set on the forest floor would not providedata representative of insect assemblages in the forest canopyFor this reason white-striped freetail bat (Tadarida australisGray) a high-flying bat was excluded from all regressionanalyses

Results

Bat fauna

In all 17 025 bat calls were recorded across all habitatsrepresenting 13 species and two species groups of which sixare currently listed as threatened under the NSW ThreatenedSpecies Conservation Act 1995 The forest habitat sustained allrecorded taxa whereas 12 and 11 taxa were present in saltmarshand urban habitats respectively (Table 1) In all 13 190 (775)2237 (131) and 1598 (94) bat passeswere recorded in foresturban and saltmarsh habitats respectively

Four taxa (Gouldrsquos wattled bat Chalinolobus gouldii Grayeastern freetail bat Mormopterus sp 2 Peters T australis andVespadelus spp) represented ~67 and ~56 of all activityrecorded in saltmarsh and urban habitats respectively (Table 1)In the forest habitat three taxa (C gouldii chocolate wattled batC morio Gray and Vespadelus spp) contributed ~77 of allrecorded activity (Table 1)

Mean nightly species diversity (measured as species richness)was significantly different among habitats (F = 5699 P = 0009)

Tab

le1

Meansenigh

tlyba

tactivity

(untransform

edda

ta)of

individu

alspeciesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletterswith

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Chalin

olob

usdw

yeri

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

02plusmn02

01plusmn01

01plusmn01

01plusmn01

01plusmn01

Cg

ouldii

72plusmn20

60plusmn17

66plusmn13

70plusmn22

112plusmn47

92plusmn26

172plusmn89

91plusmn56

129plusmn51

105plusmn31

88plusmn24

96plusmn20

Cm

orio

01plusmn01

01plusmn01

136plusmn13

77plusmn71

105plusmn7

45plusmn43

26plusmn24

35plusmn24

Falsistrellu

stasm

aniensis

02plusmn01

01plusmn01

01plusmn01

01plusmn01

Kerivou

lapa

puensis

01plusmn01

lt01plusmnlt0

1Miniopterus

australis

03plusmn02

02plusmn01

03plusmn02

01plusmn01

17plusmn07

22plusmn17

20plusmn09

07plusmn03

08plusmn06

07plusmn03

Mischreibersiioceanensis

03plusmn02

01plusmn01

02plusmn01

03plusmn02

03plusmn01

03plusmn01

01plusmn01

03plusmn02

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Mormop

terussp2

69plusmn12

33plusmn08

50plusmn08

44plusmn15

28plusmn11

36plusmn09

15plusmn08

07plusmn05

10plusmn04

43plusmn08

23plusmn05

32plusmn05

Nyctoph

ilusspp

01plusmn01

01plusmn00

01plusmn01

01plusmn0

10plusmn02

01plusmn01

06plusmn01

04plusmn01

01plusmn01

02plusmn01

Rhino

loph

usmegap

hyllu

s01plusmn01

01plusmn0

01plusmn01

02plusmn01

02plusmn01

01plusmn01

01plusmn01

Scoteana

xrueppellii

02plusmn01

01plusmn00

08plusmn07

04plusmn03

02plusmn01

01plusmn01

04plusmn02

02plusmn01

Scotorepensorion

02plusmn01

01plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Tadaridaau

stralis

23plusmn06

12plusmn04

17plusmn04

22plusmn09

11plusmn03

16plusmn05

10plusmn05

04plusmn02

07plusmn02

19plusmn04

09plusmn02

13plusmn02

Vespadelusda

rlington

i01plusmn01

01plusmn00

04plusmn03

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

Vespadelusspp

117plusmn86

31plusmn16

71plusmn41

25plusmn08

17plusmn06

21plusmn05

2112plusmn85

214

77plusmn67

617

76plusmn52

675

2plusmn33

950

8plusmn25

562

3plusmn20

7Total

385plusmn14

617

6plusmn44

274plusmn75

465plusmn19

935

8plusmn10

740

9plusmn10

733

87plusmn88

820

88plusmn81

326

99plusmn60

314

12plusmn41

487

4plusmn31

311

27plusmn25

6Species

richness

60plusmn03

54plusmn07

57abplusmn04

50plusmn06

41plusmn05

45a

plusmn04

80plusmn07

53plusmn06

66b

plusmn06

63plusmn04

50plusmn04

56plusmn03

14 Wildlife Research L Gonsalves et al

and tides (F = 7246 P = 0012) with greater species diversityrecorded in forest than in urban habitat (P= 0007) (Table 1)

Nightly bat activity (number of bat passes per night) wassignificantly different among habitats (F= 20141 P lt 0001)with significantly greater activity recorded in forest than insaltmarsh and urban habitats respectively (P lt 0001 Fig 2)

The activity ofMo sp 2 (F = 14108 P lt 0001) T australis(F = 3636 P = 0040) and Vespadelus spp (F = 70180P lt 0001) differed significantly among habitats KruskalndashWallis ANOVA revealed that the activity of C morio(H= 24162 Plt 0001) and little bent-wing bat (Miniopterus

australis Tommes) (H= 18160 Plt 0001) differedsignificantly among habitats Bonferroni comparisonsindicated that C morio Mi australis and Vespadelusspp were significantly more active in forest than in saltmarsh(P= 005 P = 0011 Plt 0001 Fig 3a b e) and urban habitats(P= 0002P= 0001P lt 0001 Fig 3ab e)Tadarida australiswas significantly more active in saltmarsh than in forest habitat(P= 0050 Fig 3d) whereas Mo sp 2 was significantly moreactive in saltmarsh (P lt 0001) andurban (P= 0001)habitats thanin the forest habitat (Fig 3c)

Although nightly bat activity did not differ among tidalcycles the activity of individual species did with significantlygreater activity recorded forMo sp 2 (F = 6339 P = 0018) andT australis (F= 5068 P = 0033) during neap tides (Fig 4a b)

Bat foraging activity

In all 268 feeding buzzes (17 of all calls) were recordedacross all habitats with 55 8 and 205 buzzes detected insaltmarsh urban and forest habitats respectively Proportionalfeeding activity differed significantly among habitats (df = 2c2 = 33600 Plt 0001) representing 40 04 and 16 ofcalls recorded in saltmarsh urban and forest habitatsrespectively Although the number of feeding buzzes recordedduring neap tides (159) was greater than spring tides (109)proportional feeding activity did not differ between the tidalcycles

Feeding buzzes were recorded for three species (C gouldii ndash15 Mi australis ndash 3 Mo sp 2 ndash 9) and one species group

14C morio

T australis Vespadelus spp

Mi australisMo sp 2

12(a)

(d ) (e)

(b) (c)

10

08

06

04

02 a a

a

aa

ab

b

b

aa

a

a

b b

b

00

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pass

es n

ight

ndash1)

plusmn S

E 08

20

15

10

05

00

10

06

04

02

00

08

10

12 6

5

4

3

2

1

0

06

04

02

00Saltmarsh Urban UrbanForest ForestSaltmarsh

Urban ForestSaltmarsh

Fig 3 Mean nightly bat activity in each habitat (a) Chalinolobus morio (b) Miniopterus australis (c) Mormopterus sp 2 (d) Tadarida australis(e) Vespadelus spp Means denoted by different letters are significantly different from one another

6

5

4

3

2

1

0Saltmarsh

Nig

htly

bat

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

aa

b

Urban Forest

Fig 2 Nightly bat activity recorded in each habitat Means denoted bydifferent letters are significantly different from one another

Do mosquitoes influence bat activity Wildlife Research 15

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

(Bouddi National Park 1189 ha) and five smaller nature reserves(Cockle Bay Nature Reserve 685 ha Rileys Island NatureReserve 457 ha Pelican Island Nature Reserve 40 haSaratoga Island Nature Reserve 2 ha) The national park andnature reserves support populations of hollow- and cave-roosting insectivorous bats including six threatened specieslisted under the NSW Threatened Species Conservation Act1995 (Payne 2006) Coastal saltmarsh urban areas and forestsrepresent three major habitats in the study area These habitatsare grossly different from one another and characteristics ofeach of these habitats are described below

Coastal saltmarsh habitat is characterised by low-growingsalt-tolerant succulent herbs such as samphire (Sarcocorniaquinqueflora (Bunge ex Ung-Sternb) AJScott) and creepingbrookweed (Samolus repens (JRForst amp GForst) Pers)Although saltmarsh lacks trees a small number of greymangrove shrubs (Avicennia marina (Forsk) Vierh) (lt3mhigh) occurred in patches as a result of the landwardtransgression of mangroves (Saintilan and Williams 1999)This vegetation community represents important larval habitatsfor many estuarine mosquito species including Ae vigilaxHexham grey (Ae alternans Westwood) and saltmarshculex (Culex sitiens Wiedemann) (Webb and Russell 2009)Additionally coastal saltmarsh communities have been foundto supportmoderately high levels of bat activity (Lamb2009) andrepresent important foraging habitats for bats (Belbaseacute 2005)

Urban habitat is characterised primarily by residential areasthat include dwellings and structures associated with residential

areas such as schools roads and street lights Urban habitatsprovide a range of suitable larval habitats for urban mosquitospecies such as domestic container mosquito (Ae notoscriptusSkuse) brown house mosquito (Cx quiquefasciatus Say) andundergroundmosquito (CxmolestusForskal) (Webb andRussell2009) Urban areas also sustain a diverse range of bat species andtypically support lower levels of bat activity (Avila-Flores andFenton 2005 Scanlon and Petit 2008 Hourigan et al 2010Threlfall et al 2011 2012) However species diversity andactivity levels within urban habitats vary with the degree ofurbanisation (Hourigan et al 2006 Threlfall et al 20112012) Although no attempt has been made to define the urbanhabitat on the basis of the degree of urbanisation residentialdensity in the overall study area was relatively low (25 dwellingshandash1) and could be classified as suburban The close proximity ofurban areas to saltmarsh and forest habitats meant that withinthe urban habitat patches of moderately vegetated areas werepresent Although attempts were made to avoid sampling nearthese patches thiswas not always possible given the small extentof urban spacewithin the study area aswell as limitations imposedby landowners All sampling was undertaken in a mannerthat attempted to minimise the influence of these vegetatedareas (ie detectors were oriented away from vegetation andarthropod sampling was conducted at the furthest practicallypossible distance away fromvegetation being ~30ndash420maway)

The forest habitat is situated on an escarpment thatstraddles the landward side of the urban habitat Sampling ofthis habitat was undertaken in Narrabeen Coastal Blackbutt

Saltmarsh

Urban

Forest

Block 0 05 1 Kilometers

Fig 1 Satellite image of study area (adapted from Google Earth) Sampling location star = saltmarsh triangle = urbandoughnut = forest in each blocked site

12 Wildlife Research L Gonsalves et al

Forest within Bouddi National Park Dominated by blackbutt(Eucalyptus pilularis Smith) turpentine (Syncarpia glomuliferasubsp glomulifera Smith) and bakers oak (Allocasuarinatorulosa (Aiton) LASJohnson) this vegetation communityhas a typical canopy height of 20m occurring on Narrabeensandstone that supports a sparse-to-moderate understoreyof shrubs and a well developed grass layer (Bell 2009) With~40 canopy cover this vegetation community can be describedas an open forest (Specht 1970) The forest habitat containsareas that provide suitable larval habitats for many floodwaterspecies including Ae multiplex Theobald Ae procax Skuseand brackish forest mosquito (Verrallina funerea Theobald)Additionally forest communities are known to sustain severalhollow- and cave-roosting bats (Payne 2006) and represent animportant habitat for foraging bats in the study area (Lamb 2009)

Study design

We surveyed insectivorous bat activity and the abundancesof mosquito fauna and other volant insect fauna at four sites(Empire Bay Cockle Bay Palmers Lane and Bensville) withinthe study area Each site was considered a block containingcorresponding saltmarsh urban and forest habitats that weresampled concurrently (Fig 1) Sites were surveyed from duskto dawn over three consecutive nights each fortnight fromDecember 2008 to April 2009 All sampling was carried out ata consistent point within each site (ie sampling sites were notshiftedwithin each site after each sampling occasion) The start ofeach fortnight coincided with a spring or a neap tide which isconsidered to have a strong influence on Ae vigilax abundance(de Little et al 2009 Kokkinn et al 2009) Data were collectedover five spring tides and four neap tides with two sites surveyedconcurrently each fortnight

Bat survey

In each habitat one Anabat SD1 detector (Titley ElectronicsBallina NSW Australia) was set at a height of 1m and at a 45

angle to the ground facing open areas (interior of saltmarshaway from structures in urban areas and along fire trails withinforested areas) Detectors recorded navigational and feedingecholocation calls of microchiropteran bats that vary fromspecies to species and can be used to differentiate among mostspeciesAll recordingswere stored on a compactflash card beforebeing uploaded to a laptop for analysis Recorded bat calls wereidentified to species where possible using the automated call-identification software AnaScheme (Gibson and Lumsden2003) in association with a key for the lower north-easternNew South Wales coastal plain (Adams et al 2010) Testingof this key revealed that 05 of all calls (n= 191) wereincorrectly identified with misidentifications restricted to callsfrom a single species (large forest bat Vespadelus darlingtoniAllen) (Adams et al 2010) Bat calls with fewer than three validpulses (ie minimum of six data points and model quality of09) were not analysed by AnaScheme Because multiple batspecies may call simultaneously calls were assigned to a speciesonly if gt50of pulses within the sequencewere attributed to thatspecies and only passeswith aminimumof three pulses classifiedto the same species were identified All calls that could not be

assigned to a bat taxonwere included in counts of total bat activitybut were labelled as lsquounidentifiedrsquo

Echolocation calls of certain species overlap to such adegree that it is not possible to differentiate among themConsequently the identification key grouped certain speciestogether (eg Gouldrsquos long-eared bat Nyctophilus gouldiTomes and lesser long-eared bat N geoffroyi Leach =Nyctophilus spp eastern forest bat V pumilus Gray easterncave bat V troughtoni Kitchener Jones amp Caputi and littleforest bat V vulturnus Thomas =Vespadelus spp) AlthoughV troughtoni calls could contribute to the activity of theVespadelus species group intensive harp trapping in the area(throughout a field season) failed to catch any V troughtoniindividuals suggesting that the activity of Vespadelus spp islikely to represent the activity of V pumilus and V vulturnusonly both of which were commonly captured in harp traps(Gonsalves 2012) All identified calls were screened manuallyfor feeding buzzes ndash a rapid increase in pulse-repetition rateslope frequencyand speed (associatedwithpursuit and captureofprey Griffin et al 1960 Pennay et al 2004) For each detectorand each night the number of bat passes and number of feedingbuzzes for each species was tabulated

Prey survey

In each habitat mosquito abundance was surveyed nightly withtwo CO2-baited encephalitis-virus surveillance (EVS) traps(Rohe and Fall 1979) (Australian Entomological SuppliesBangalow NSW Australia) whereas other aerial insect faunawere sampled with one light trap (Australian EntomologicalSupplies Bangalow NSW Australia) All traps were set at aminimumdistance of 10m frombat detectors Trapswere set nearstructures (isolated mangroves within coastal saltmarsh gardenshrubs in urban areas and vegetation along the edge of a fire trailin forested areas) in each habitat that allowed EVS traps to besuspended Mosquito collections were identified to speciesaccording to keys (Russell 1996) and the abundance of eachspecies was recorded All light-trap specimens were sorted intothree insect orders (Lepidoptera Coleoptera Diptera) with anyother specimens pooled into an lsquootherrsquo category These insectgroups were then further sorted by size into four size classes(tip of head to tip of abdomen) (lt5mm 5ndash9mm 10ndash14mm andgt14mm) Counts of all insects thenwere carried out and recordedfor each night of trapping in each habitat Insects were oven-driedat 60C for a minimum of 48 h until a constant weight could berecorded (to nearest 1 105 g) For samples withmore than 100insects in a lt5-mm size class the mass of the total sample wasused along with regression equations (calculated for each taxonby using count and dry-weight data obtained for all other samplesof insects lt5mm) to estimate the abundance of the sample

Data analyses

Prior to analysis all collected data were log-transformed andaveraged across consecutive nights for each site during eachfortnight Although dry-weight data were available for all insecttaxa and size classes only abundance values were used inanalyses to allow for comparison with Ae vigilax for whichonly abundance values were available A repeated-measuresmixed-model ANOVA was used to test for effects of habitat

Do mosquitoes influence bat activity Wildlife Research 13

(saltmarshurbanforest) tidal cycle (neapspring) and allinteractions on mean nightly bat activity the activity of thecommonly recorded species (representing gt050 of total batactivity) Ae vigilax abundance and the abundance of othervolant insects An autoregressive order-one covariancestructure was used for the repeated factor (tidal cycle) in eachanalysis because this covariance structure assumes thatmeasurements taken close to one another in time will be moreclosely correlated than measurements taken at greater intervalsin time Comparisons of main effects were Bonferroni correctedfor multiple comparisons For each dependent variable if datawere not normally distributed a KruskalndashWallis test was insteadused to examine the effect of each independent variable

A goodness of fit chi-square test was used to compareproportional feeding activity (proportion of bat callscontaining feeding buzzes) and the proportional feedingactivity of individual species between habitats and tidal cyclewhereas best-subsets regression analysis was used to examinerelationships among the abundances of non-mosquito prey(lepidopterans coleopterans dipterans other insects all taxapooled insects lt5mm insects 5ndash9mm insects 10ndash14mm andinsects gt14mm) Ae vigilax abundance and bat activity aswell as the activity of the commonly recorded bat species(representing gt050 of total bat activity) No climaticvariables (eg temperature humidity wind) were incorporatedinto regression models Selection of models for each dependentvariable was based on Akaike information criteria scorescorrected for small sample sizes (AICc) Since vegetationclutter influences prey detectability (Adams et al 2009Rainho et al 2010) analyses were conducted for each habitatseparately Given insect abundances vary with height withinforests (Adams et al 2009) it was considered that preytrapped in light traps set on the forest floor would not providedata representative of insect assemblages in the forest canopyFor this reason white-striped freetail bat (Tadarida australisGray) a high-flying bat was excluded from all regressionanalyses

Results

Bat fauna

In all 17 025 bat calls were recorded across all habitatsrepresenting 13 species and two species groups of which sixare currently listed as threatened under the NSW ThreatenedSpecies Conservation Act 1995 The forest habitat sustained allrecorded taxa whereas 12 and 11 taxa were present in saltmarshand urban habitats respectively (Table 1) In all 13 190 (775)2237 (131) and 1598 (94) bat passeswere recorded in foresturban and saltmarsh habitats respectively

Four taxa (Gouldrsquos wattled bat Chalinolobus gouldii Grayeastern freetail bat Mormopterus sp 2 Peters T australis andVespadelus spp) represented ~67 and ~56 of all activityrecorded in saltmarsh and urban habitats respectively (Table 1)In the forest habitat three taxa (C gouldii chocolate wattled batC morio Gray and Vespadelus spp) contributed ~77 of allrecorded activity (Table 1)

Mean nightly species diversity (measured as species richness)was significantly different among habitats (F = 5699 P = 0009)

Tab

le1

Meansenigh

tlyba

tactivity

(untransform

edda

ta)of

individu

alspeciesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletterswith

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Chalin

olob

usdw

yeri

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

02plusmn02

01plusmn01

01plusmn01

01plusmn01

01plusmn01

Cg

ouldii

72plusmn20

60plusmn17

66plusmn13

70plusmn22

112plusmn47

92plusmn26

172plusmn89

91plusmn56

129plusmn51

105plusmn31

88plusmn24

96plusmn20

Cm

orio

01plusmn01

01plusmn01

136plusmn13

77plusmn71

105plusmn7

45plusmn43

26plusmn24

35plusmn24

Falsistrellu

stasm

aniensis

02plusmn01

01plusmn01

01plusmn01

01plusmn01

Kerivou

lapa

puensis

01plusmn01

lt01plusmnlt0

1Miniopterus

australis

03plusmn02

02plusmn01

03plusmn02

01plusmn01

17plusmn07

22plusmn17

20plusmn09

07plusmn03

08plusmn06

07plusmn03

Mischreibersiioceanensis

03plusmn02

01plusmn01

02plusmn01

03plusmn02

03plusmn01

03plusmn01

01plusmn01

03plusmn02

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Mormop

terussp2

69plusmn12

33plusmn08

50plusmn08

44plusmn15

28plusmn11

36plusmn09

15plusmn08

07plusmn05

10plusmn04

43plusmn08

23plusmn05

32plusmn05

Nyctoph

ilusspp

01plusmn01

01plusmn00

01plusmn01

01plusmn0

10plusmn02

01plusmn01

06plusmn01

04plusmn01

01plusmn01

02plusmn01

Rhino

loph

usmegap

hyllu

s01plusmn01

01plusmn0

01plusmn01

02plusmn01

02plusmn01

01plusmn01

01plusmn01

Scoteana

xrueppellii

02plusmn01

01plusmn00

08plusmn07

04plusmn03

02plusmn01

01plusmn01

04plusmn02

02plusmn01

Scotorepensorion

02plusmn01

01plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Tadaridaau

stralis

23plusmn06

12plusmn04

17plusmn04

22plusmn09

11plusmn03

16plusmn05

10plusmn05

04plusmn02

07plusmn02

19plusmn04

09plusmn02

13plusmn02

Vespadelusda

rlington

i01plusmn01

01plusmn00

04plusmn03

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

Vespadelusspp

117plusmn86

31plusmn16

71plusmn41

25plusmn08

17plusmn06

21plusmn05

2112plusmn85

214

77plusmn67

617

76plusmn52

675

2plusmn33

950

8plusmn25

562

3plusmn20

7Total

385plusmn14

617

6plusmn44

274plusmn75

465plusmn19

935

8plusmn10

740

9plusmn10

733

87plusmn88

820

88plusmn81

326

99plusmn60

314

12plusmn41

487

4plusmn31

311

27plusmn25

6Species

richness

60plusmn03

54plusmn07

57abplusmn04

50plusmn06

41plusmn05

45a

plusmn04

80plusmn07

53plusmn06

66b

plusmn06

63plusmn04

50plusmn04

56plusmn03

14 Wildlife Research L Gonsalves et al

and tides (F = 7246 P = 0012) with greater species diversityrecorded in forest than in urban habitat (P= 0007) (Table 1)

Nightly bat activity (number of bat passes per night) wassignificantly different among habitats (F= 20141 P lt 0001)with significantly greater activity recorded in forest than insaltmarsh and urban habitats respectively (P lt 0001 Fig 2)

The activity ofMo sp 2 (F = 14108 P lt 0001) T australis(F = 3636 P = 0040) and Vespadelus spp (F = 70180P lt 0001) differed significantly among habitats KruskalndashWallis ANOVA revealed that the activity of C morio(H= 24162 Plt 0001) and little bent-wing bat (Miniopterus

australis Tommes) (H= 18160 Plt 0001) differedsignificantly among habitats Bonferroni comparisonsindicated that C morio Mi australis and Vespadelusspp were significantly more active in forest than in saltmarsh(P= 005 P = 0011 Plt 0001 Fig 3a b e) and urban habitats(P= 0002P= 0001P lt 0001 Fig 3ab e)Tadarida australiswas significantly more active in saltmarsh than in forest habitat(P= 0050 Fig 3d) whereas Mo sp 2 was significantly moreactive in saltmarsh (P lt 0001) andurban (P= 0001)habitats thanin the forest habitat (Fig 3c)

Although nightly bat activity did not differ among tidalcycles the activity of individual species did with significantlygreater activity recorded forMo sp 2 (F = 6339 P = 0018) andT australis (F= 5068 P = 0033) during neap tides (Fig 4a b)

Bat foraging activity

In all 268 feeding buzzes (17 of all calls) were recordedacross all habitats with 55 8 and 205 buzzes detected insaltmarsh urban and forest habitats respectively Proportionalfeeding activity differed significantly among habitats (df = 2c2 = 33600 Plt 0001) representing 40 04 and 16 ofcalls recorded in saltmarsh urban and forest habitatsrespectively Although the number of feeding buzzes recordedduring neap tides (159) was greater than spring tides (109)proportional feeding activity did not differ between the tidalcycles

Feeding buzzes were recorded for three species (C gouldii ndash15 Mi australis ndash 3 Mo sp 2 ndash 9) and one species group

14C morio

T australis Vespadelus spp

Mi australisMo sp 2

12(a)

(d ) (e)

(b) (c)

10

08

06

04

02 a a

a

aa

ab

b

b

aa

a

a

b b

b

00

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pass

es n

ight

ndash1)

plusmn S

E 08

20

15

10

05

00

10

06

04

02

00

08

10

12 6

5

4

3

2

1

0

06

04

02

00Saltmarsh Urban UrbanForest ForestSaltmarsh

Urban ForestSaltmarsh

Fig 3 Mean nightly bat activity in each habitat (a) Chalinolobus morio (b) Miniopterus australis (c) Mormopterus sp 2 (d) Tadarida australis(e) Vespadelus spp Means denoted by different letters are significantly different from one another

6

5

4

3

2

1

0Saltmarsh

Nig

htly

bat

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

aa

b

Urban Forest

Fig 2 Nightly bat activity recorded in each habitat Means denoted bydifferent letters are significantly different from one another

Do mosquitoes influence bat activity Wildlife Research 15

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

Forest within Bouddi National Park Dominated by blackbutt(Eucalyptus pilularis Smith) turpentine (Syncarpia glomuliferasubsp glomulifera Smith) and bakers oak (Allocasuarinatorulosa (Aiton) LASJohnson) this vegetation communityhas a typical canopy height of 20m occurring on Narrabeensandstone that supports a sparse-to-moderate understoreyof shrubs and a well developed grass layer (Bell 2009) With~40 canopy cover this vegetation community can be describedas an open forest (Specht 1970) The forest habitat containsareas that provide suitable larval habitats for many floodwaterspecies including Ae multiplex Theobald Ae procax Skuseand brackish forest mosquito (Verrallina funerea Theobald)Additionally forest communities are known to sustain severalhollow- and cave-roosting bats (Payne 2006) and represent animportant habitat for foraging bats in the study area (Lamb 2009)

Study design

We surveyed insectivorous bat activity and the abundancesof mosquito fauna and other volant insect fauna at four sites(Empire Bay Cockle Bay Palmers Lane and Bensville) withinthe study area Each site was considered a block containingcorresponding saltmarsh urban and forest habitats that weresampled concurrently (Fig 1) Sites were surveyed from duskto dawn over three consecutive nights each fortnight fromDecember 2008 to April 2009 All sampling was carried out ata consistent point within each site (ie sampling sites were notshiftedwithin each site after each sampling occasion) The start ofeach fortnight coincided with a spring or a neap tide which isconsidered to have a strong influence on Ae vigilax abundance(de Little et al 2009 Kokkinn et al 2009) Data were collectedover five spring tides and four neap tides with two sites surveyedconcurrently each fortnight

Bat survey

In each habitat one Anabat SD1 detector (Titley ElectronicsBallina NSW Australia) was set at a height of 1m and at a 45

angle to the ground facing open areas (interior of saltmarshaway from structures in urban areas and along fire trails withinforested areas) Detectors recorded navigational and feedingecholocation calls of microchiropteran bats that vary fromspecies to species and can be used to differentiate among mostspeciesAll recordingswere stored on a compactflash card beforebeing uploaded to a laptop for analysis Recorded bat calls wereidentified to species where possible using the automated call-identification software AnaScheme (Gibson and Lumsden2003) in association with a key for the lower north-easternNew South Wales coastal plain (Adams et al 2010) Testingof this key revealed that 05 of all calls (n= 191) wereincorrectly identified with misidentifications restricted to callsfrom a single species (large forest bat Vespadelus darlingtoniAllen) (Adams et al 2010) Bat calls with fewer than three validpulses (ie minimum of six data points and model quality of09) were not analysed by AnaScheme Because multiple batspecies may call simultaneously calls were assigned to a speciesonly if gt50of pulses within the sequencewere attributed to thatspecies and only passeswith aminimumof three pulses classifiedto the same species were identified All calls that could not be

assigned to a bat taxonwere included in counts of total bat activitybut were labelled as lsquounidentifiedrsquo

Echolocation calls of certain species overlap to such adegree that it is not possible to differentiate among themConsequently the identification key grouped certain speciestogether (eg Gouldrsquos long-eared bat Nyctophilus gouldiTomes and lesser long-eared bat N geoffroyi Leach =Nyctophilus spp eastern forest bat V pumilus Gray easterncave bat V troughtoni Kitchener Jones amp Caputi and littleforest bat V vulturnus Thomas =Vespadelus spp) AlthoughV troughtoni calls could contribute to the activity of theVespadelus species group intensive harp trapping in the area(throughout a field season) failed to catch any V troughtoniindividuals suggesting that the activity of Vespadelus spp islikely to represent the activity of V pumilus and V vulturnusonly both of which were commonly captured in harp traps(Gonsalves 2012) All identified calls were screened manuallyfor feeding buzzes ndash a rapid increase in pulse-repetition rateslope frequencyand speed (associatedwithpursuit and captureofprey Griffin et al 1960 Pennay et al 2004) For each detectorand each night the number of bat passes and number of feedingbuzzes for each species was tabulated

Prey survey

In each habitat mosquito abundance was surveyed nightly withtwo CO2-baited encephalitis-virus surveillance (EVS) traps(Rohe and Fall 1979) (Australian Entomological SuppliesBangalow NSW Australia) whereas other aerial insect faunawere sampled with one light trap (Australian EntomologicalSupplies Bangalow NSW Australia) All traps were set at aminimumdistance of 10m frombat detectors Trapswere set nearstructures (isolated mangroves within coastal saltmarsh gardenshrubs in urban areas and vegetation along the edge of a fire trailin forested areas) in each habitat that allowed EVS traps to besuspended Mosquito collections were identified to speciesaccording to keys (Russell 1996) and the abundance of eachspecies was recorded All light-trap specimens were sorted intothree insect orders (Lepidoptera Coleoptera Diptera) with anyother specimens pooled into an lsquootherrsquo category These insectgroups were then further sorted by size into four size classes(tip of head to tip of abdomen) (lt5mm 5ndash9mm 10ndash14mm andgt14mm) Counts of all insects thenwere carried out and recordedfor each night of trapping in each habitat Insects were oven-driedat 60C for a minimum of 48 h until a constant weight could berecorded (to nearest 1 105 g) For samples withmore than 100insects in a lt5-mm size class the mass of the total sample wasused along with regression equations (calculated for each taxonby using count and dry-weight data obtained for all other samplesof insects lt5mm) to estimate the abundance of the sample

Data analyses

Prior to analysis all collected data were log-transformed andaveraged across consecutive nights for each site during eachfortnight Although dry-weight data were available for all insecttaxa and size classes only abundance values were used inanalyses to allow for comparison with Ae vigilax for whichonly abundance values were available A repeated-measuresmixed-model ANOVA was used to test for effects of habitat

Do mosquitoes influence bat activity Wildlife Research 13

(saltmarshurbanforest) tidal cycle (neapspring) and allinteractions on mean nightly bat activity the activity of thecommonly recorded species (representing gt050 of total batactivity) Ae vigilax abundance and the abundance of othervolant insects An autoregressive order-one covariancestructure was used for the repeated factor (tidal cycle) in eachanalysis because this covariance structure assumes thatmeasurements taken close to one another in time will be moreclosely correlated than measurements taken at greater intervalsin time Comparisons of main effects were Bonferroni correctedfor multiple comparisons For each dependent variable if datawere not normally distributed a KruskalndashWallis test was insteadused to examine the effect of each independent variable

A goodness of fit chi-square test was used to compareproportional feeding activity (proportion of bat callscontaining feeding buzzes) and the proportional feedingactivity of individual species between habitats and tidal cyclewhereas best-subsets regression analysis was used to examinerelationships among the abundances of non-mosquito prey(lepidopterans coleopterans dipterans other insects all taxapooled insects lt5mm insects 5ndash9mm insects 10ndash14mm andinsects gt14mm) Ae vigilax abundance and bat activity aswell as the activity of the commonly recorded bat species(representing gt050 of total bat activity) No climaticvariables (eg temperature humidity wind) were incorporatedinto regression models Selection of models for each dependentvariable was based on Akaike information criteria scorescorrected for small sample sizes (AICc) Since vegetationclutter influences prey detectability (Adams et al 2009Rainho et al 2010) analyses were conducted for each habitatseparately Given insect abundances vary with height withinforests (Adams et al 2009) it was considered that preytrapped in light traps set on the forest floor would not providedata representative of insect assemblages in the forest canopyFor this reason white-striped freetail bat (Tadarida australisGray) a high-flying bat was excluded from all regressionanalyses

Results

Bat fauna

In all 17 025 bat calls were recorded across all habitatsrepresenting 13 species and two species groups of which sixare currently listed as threatened under the NSW ThreatenedSpecies Conservation Act 1995 The forest habitat sustained allrecorded taxa whereas 12 and 11 taxa were present in saltmarshand urban habitats respectively (Table 1) In all 13 190 (775)2237 (131) and 1598 (94) bat passeswere recorded in foresturban and saltmarsh habitats respectively

Four taxa (Gouldrsquos wattled bat Chalinolobus gouldii Grayeastern freetail bat Mormopterus sp 2 Peters T australis andVespadelus spp) represented ~67 and ~56 of all activityrecorded in saltmarsh and urban habitats respectively (Table 1)In the forest habitat three taxa (C gouldii chocolate wattled batC morio Gray and Vespadelus spp) contributed ~77 of allrecorded activity (Table 1)

Mean nightly species diversity (measured as species richness)was significantly different among habitats (F = 5699 P = 0009)

Tab

le1

Meansenigh

tlyba

tactivity

(untransform

edda

ta)of

individu

alspeciesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletterswith

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Chalin

olob

usdw

yeri

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

02plusmn02

01plusmn01

01plusmn01

01plusmn01

01plusmn01

Cg

ouldii

72plusmn20

60plusmn17

66plusmn13

70plusmn22

112plusmn47

92plusmn26

172plusmn89

91plusmn56

129plusmn51

105plusmn31

88plusmn24

96plusmn20

Cm

orio

01plusmn01

01plusmn01

136plusmn13

77plusmn71

105plusmn7

45plusmn43

26plusmn24

35plusmn24

Falsistrellu

stasm

aniensis

02plusmn01

01plusmn01

01plusmn01

01plusmn01

Kerivou

lapa

puensis

01plusmn01

lt01plusmnlt0

1Miniopterus

australis

03plusmn02

02plusmn01

03plusmn02

01plusmn01

17plusmn07

22plusmn17

20plusmn09

07plusmn03

08plusmn06

07plusmn03

Mischreibersiioceanensis

03plusmn02

01plusmn01

02plusmn01

03plusmn02

03plusmn01

03plusmn01

01plusmn01

03plusmn02

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Mormop

terussp2

69plusmn12

33plusmn08

50plusmn08

44plusmn15

28plusmn11

36plusmn09

15plusmn08

07plusmn05

10plusmn04

43plusmn08

23plusmn05

32plusmn05

Nyctoph

ilusspp

01plusmn01

01plusmn00

01plusmn01

01plusmn0

10plusmn02

01plusmn01

06plusmn01

04plusmn01

01plusmn01

02plusmn01

Rhino

loph

usmegap

hyllu

s01plusmn01

01plusmn0

01plusmn01

02plusmn01

02plusmn01

01plusmn01

01plusmn01

Scoteana

xrueppellii

02plusmn01

01plusmn00

08plusmn07

04plusmn03

02plusmn01

01plusmn01

04plusmn02

02plusmn01

Scotorepensorion

02plusmn01

01plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Tadaridaau

stralis

23plusmn06

12plusmn04

17plusmn04

22plusmn09

11plusmn03

16plusmn05

10plusmn05

04plusmn02

07plusmn02

19plusmn04

09plusmn02

13plusmn02

Vespadelusda

rlington

i01plusmn01

01plusmn00

04plusmn03

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

Vespadelusspp

117plusmn86

31plusmn16

71plusmn41

25plusmn08

17plusmn06

21plusmn05

2112plusmn85

214

77plusmn67

617

76plusmn52

675

2plusmn33

950

8plusmn25

562

3plusmn20

7Total

385plusmn14

617

6plusmn44

274plusmn75

465plusmn19

935

8plusmn10

740

9plusmn10

733

87plusmn88

820

88plusmn81

326

99plusmn60

314

12plusmn41

487

4plusmn31

311

27plusmn25

6Species

richness

60plusmn03

54plusmn07

57abplusmn04

50plusmn06

41plusmn05

45a

plusmn04

80plusmn07

53plusmn06

66b

plusmn06

63plusmn04

50plusmn04

56plusmn03

14 Wildlife Research L Gonsalves et al

and tides (F = 7246 P = 0012) with greater species diversityrecorded in forest than in urban habitat (P= 0007) (Table 1)

Nightly bat activity (number of bat passes per night) wassignificantly different among habitats (F= 20141 P lt 0001)with significantly greater activity recorded in forest than insaltmarsh and urban habitats respectively (P lt 0001 Fig 2)

The activity ofMo sp 2 (F = 14108 P lt 0001) T australis(F = 3636 P = 0040) and Vespadelus spp (F = 70180P lt 0001) differed significantly among habitats KruskalndashWallis ANOVA revealed that the activity of C morio(H= 24162 Plt 0001) and little bent-wing bat (Miniopterus

australis Tommes) (H= 18160 Plt 0001) differedsignificantly among habitats Bonferroni comparisonsindicated that C morio Mi australis and Vespadelusspp were significantly more active in forest than in saltmarsh(P= 005 P = 0011 Plt 0001 Fig 3a b e) and urban habitats(P= 0002P= 0001P lt 0001 Fig 3ab e)Tadarida australiswas significantly more active in saltmarsh than in forest habitat(P= 0050 Fig 3d) whereas Mo sp 2 was significantly moreactive in saltmarsh (P lt 0001) andurban (P= 0001)habitats thanin the forest habitat (Fig 3c)

Although nightly bat activity did not differ among tidalcycles the activity of individual species did with significantlygreater activity recorded forMo sp 2 (F = 6339 P = 0018) andT australis (F= 5068 P = 0033) during neap tides (Fig 4a b)

Bat foraging activity

In all 268 feeding buzzes (17 of all calls) were recordedacross all habitats with 55 8 and 205 buzzes detected insaltmarsh urban and forest habitats respectively Proportionalfeeding activity differed significantly among habitats (df = 2c2 = 33600 Plt 0001) representing 40 04 and 16 ofcalls recorded in saltmarsh urban and forest habitatsrespectively Although the number of feeding buzzes recordedduring neap tides (159) was greater than spring tides (109)proportional feeding activity did not differ between the tidalcycles

Feeding buzzes were recorded for three species (C gouldii ndash15 Mi australis ndash 3 Mo sp 2 ndash 9) and one species group

14C morio

T australis Vespadelus spp

Mi australisMo sp 2

12(a)

(d ) (e)

(b) (c)

10

08

06

04

02 a a

a

aa

ab

b

b

aa

a

a

b b

b

00

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pass

es n

ight

ndash1)

plusmn S

E 08

20

15

10

05

00

10

06

04

02

00

08

10

12 6

5

4

3

2

1

0

06

04

02

00Saltmarsh Urban UrbanForest ForestSaltmarsh

Urban ForestSaltmarsh

Fig 3 Mean nightly bat activity in each habitat (a) Chalinolobus morio (b) Miniopterus australis (c) Mormopterus sp 2 (d) Tadarida australis(e) Vespadelus spp Means denoted by different letters are significantly different from one another

6

5

4

3

2

1

0Saltmarsh

Nig

htly

bat

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

aa

b

Urban Forest

Fig 2 Nightly bat activity recorded in each habitat Means denoted bydifferent letters are significantly different from one another

Do mosquitoes influence bat activity Wildlife Research 15

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

(saltmarshurbanforest) tidal cycle (neapspring) and allinteractions on mean nightly bat activity the activity of thecommonly recorded species (representing gt050 of total batactivity) Ae vigilax abundance and the abundance of othervolant insects An autoregressive order-one covariancestructure was used for the repeated factor (tidal cycle) in eachanalysis because this covariance structure assumes thatmeasurements taken close to one another in time will be moreclosely correlated than measurements taken at greater intervalsin time Comparisons of main effects were Bonferroni correctedfor multiple comparisons For each dependent variable if datawere not normally distributed a KruskalndashWallis test was insteadused to examine the effect of each independent variable

A goodness of fit chi-square test was used to compareproportional feeding activity (proportion of bat callscontaining feeding buzzes) and the proportional feedingactivity of individual species between habitats and tidal cyclewhereas best-subsets regression analysis was used to examinerelationships among the abundances of non-mosquito prey(lepidopterans coleopterans dipterans other insects all taxapooled insects lt5mm insects 5ndash9mm insects 10ndash14mm andinsects gt14mm) Ae vigilax abundance and bat activity aswell as the activity of the commonly recorded bat species(representing gt050 of total bat activity) No climaticvariables (eg temperature humidity wind) were incorporatedinto regression models Selection of models for each dependentvariable was based on Akaike information criteria scorescorrected for small sample sizes (AICc) Since vegetationclutter influences prey detectability (Adams et al 2009Rainho et al 2010) analyses were conducted for each habitatseparately Given insect abundances vary with height withinforests (Adams et al 2009) it was considered that preytrapped in light traps set on the forest floor would not providedata representative of insect assemblages in the forest canopyFor this reason white-striped freetail bat (Tadarida australisGray) a high-flying bat was excluded from all regressionanalyses

Results

Bat fauna

In all 17 025 bat calls were recorded across all habitatsrepresenting 13 species and two species groups of which sixare currently listed as threatened under the NSW ThreatenedSpecies Conservation Act 1995 The forest habitat sustained allrecorded taxa whereas 12 and 11 taxa were present in saltmarshand urban habitats respectively (Table 1) In all 13 190 (775)2237 (131) and 1598 (94) bat passeswere recorded in foresturban and saltmarsh habitats respectively

Four taxa (Gouldrsquos wattled bat Chalinolobus gouldii Grayeastern freetail bat Mormopterus sp 2 Peters T australis andVespadelus spp) represented ~67 and ~56 of all activityrecorded in saltmarsh and urban habitats respectively (Table 1)In the forest habitat three taxa (C gouldii chocolate wattled batC morio Gray and Vespadelus spp) contributed ~77 of allrecorded activity (Table 1)

Mean nightly species diversity (measured as species richness)was significantly different among habitats (F = 5699 P = 0009)

Tab

le1

Meansenigh

tlyba

tactivity

(untransform

edda

ta)of

individu

alspeciesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletterswith

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Chalin

olob

usdw

yeri

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

02plusmn02

01plusmn01

01plusmn01

01plusmn01

01plusmn01

Cg

ouldii

72plusmn20

60plusmn17

66plusmn13

70plusmn22

112plusmn47

92plusmn26

172plusmn89

91plusmn56

129plusmn51

105plusmn31

88plusmn24

96plusmn20

Cm

orio

01plusmn01

01plusmn01

136plusmn13

77plusmn71

105plusmn7

45plusmn43

26plusmn24

35plusmn24

Falsistrellu

stasm

aniensis

02plusmn01

01plusmn01

01plusmn01

01plusmn01

Kerivou

lapa

puensis

01plusmn01

lt01plusmnlt0

1Miniopterus

australis

03plusmn02

02plusmn01

03plusmn02

01plusmn01

17plusmn07

22plusmn17

20plusmn09

07plusmn03

08plusmn06

07plusmn03

Mischreibersiioceanensis

03plusmn02

01plusmn01

02plusmn01

03plusmn02

03plusmn01

03plusmn01

01plusmn01

03plusmn02

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Mormop

terussp2

69plusmn12

33plusmn08

50plusmn08

44plusmn15

28plusmn11

36plusmn09

15plusmn08

07plusmn05

10plusmn04

43plusmn08

23plusmn05

32plusmn05

Nyctoph

ilusspp

01plusmn01

01plusmn00

01plusmn01

01plusmn0

10plusmn02

01plusmn01

06plusmn01

04plusmn01

01plusmn01

02plusmn01

Rhino

loph

usmegap

hyllu

s01plusmn01

01plusmn0

01plusmn01

02plusmn01

02plusmn01

01plusmn01

01plusmn01

Scoteana

xrueppellii

02plusmn01

01plusmn00

08plusmn07

04plusmn03

02plusmn01

01plusmn01

04plusmn02

02plusmn01

Scotorepensorion

02plusmn01

01plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

02plusmn01

Tadaridaau

stralis

23plusmn06

12plusmn04

17plusmn04

22plusmn09

11plusmn03

16plusmn05

10plusmn05

04plusmn02

07plusmn02

19plusmn04

09plusmn02

13plusmn02

Vespadelusda

rlington

i01plusmn01

01plusmn00

04plusmn03

01plusmn01

03plusmn02

02plusmn01

01plusmn01

01plusmn01

Vespadelusspp

117plusmn86

31plusmn16

71plusmn41

25plusmn08

17plusmn06

21plusmn05

2112plusmn85

214

77plusmn67

617

76plusmn52

675

2plusmn33

950

8plusmn25

562

3plusmn20

7Total

385plusmn14

617

6plusmn44

274plusmn75

465plusmn19

935

8plusmn10

740

9plusmn10

733

87plusmn88

820

88plusmn81

326

99plusmn60

314

12plusmn41

487

4plusmn31

311

27plusmn25

6Species

richness

60plusmn03

54plusmn07

57abplusmn04

50plusmn06

41plusmn05

45a

plusmn04

80plusmn07

53plusmn06

66b

plusmn06

63plusmn04

50plusmn04

56plusmn03

14 Wildlife Research L Gonsalves et al

and tides (F = 7246 P = 0012) with greater species diversityrecorded in forest than in urban habitat (P= 0007) (Table 1)

Nightly bat activity (number of bat passes per night) wassignificantly different among habitats (F= 20141 P lt 0001)with significantly greater activity recorded in forest than insaltmarsh and urban habitats respectively (P lt 0001 Fig 2)

The activity ofMo sp 2 (F = 14108 P lt 0001) T australis(F = 3636 P = 0040) and Vespadelus spp (F = 70180P lt 0001) differed significantly among habitats KruskalndashWallis ANOVA revealed that the activity of C morio(H= 24162 Plt 0001) and little bent-wing bat (Miniopterus

australis Tommes) (H= 18160 Plt 0001) differedsignificantly among habitats Bonferroni comparisonsindicated that C morio Mi australis and Vespadelusspp were significantly more active in forest than in saltmarsh(P= 005 P = 0011 Plt 0001 Fig 3a b e) and urban habitats(P= 0002P= 0001P lt 0001 Fig 3ab e)Tadarida australiswas significantly more active in saltmarsh than in forest habitat(P= 0050 Fig 3d) whereas Mo sp 2 was significantly moreactive in saltmarsh (P lt 0001) andurban (P= 0001)habitats thanin the forest habitat (Fig 3c)

Although nightly bat activity did not differ among tidalcycles the activity of individual species did with significantlygreater activity recorded forMo sp 2 (F = 6339 P = 0018) andT australis (F= 5068 P = 0033) during neap tides (Fig 4a b)

Bat foraging activity

In all 268 feeding buzzes (17 of all calls) were recordedacross all habitats with 55 8 and 205 buzzes detected insaltmarsh urban and forest habitats respectively Proportionalfeeding activity differed significantly among habitats (df = 2c2 = 33600 Plt 0001) representing 40 04 and 16 ofcalls recorded in saltmarsh urban and forest habitatsrespectively Although the number of feeding buzzes recordedduring neap tides (159) was greater than spring tides (109)proportional feeding activity did not differ between the tidalcycles

Feeding buzzes were recorded for three species (C gouldii ndash15 Mi australis ndash 3 Mo sp 2 ndash 9) and one species group

14C morio

T australis Vespadelus spp

Mi australisMo sp 2

12(a)

(d ) (e)

(b) (c)

10

08

06

04

02 a a

a

aa

ab

b

b

aa

a

a

b b

b

00

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pass

es n

ight

ndash1)

plusmn S

E 08

20

15

10

05

00

10

06

04

02

00

08

10

12 6

5

4

3

2

1

0

06

04

02

00Saltmarsh Urban UrbanForest ForestSaltmarsh

Urban ForestSaltmarsh

Fig 3 Mean nightly bat activity in each habitat (a) Chalinolobus morio (b) Miniopterus australis (c) Mormopterus sp 2 (d) Tadarida australis(e) Vespadelus spp Means denoted by different letters are significantly different from one another

6

5

4

3

2

1

0Saltmarsh

Nig

htly

bat

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

aa

b

Urban Forest

Fig 2 Nightly bat activity recorded in each habitat Means denoted bydifferent letters are significantly different from one another

Do mosquitoes influence bat activity Wildlife Research 15

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

and tides (F = 7246 P = 0012) with greater species diversityrecorded in forest than in urban habitat (P= 0007) (Table 1)

Nightly bat activity (number of bat passes per night) wassignificantly different among habitats (F= 20141 P lt 0001)with significantly greater activity recorded in forest than insaltmarsh and urban habitats respectively (P lt 0001 Fig 2)

The activity ofMo sp 2 (F = 14108 P lt 0001) T australis(F = 3636 P = 0040) and Vespadelus spp (F = 70180P lt 0001) differed significantly among habitats KruskalndashWallis ANOVA revealed that the activity of C morio(H= 24162 Plt 0001) and little bent-wing bat (Miniopterus

australis Tommes) (H= 18160 Plt 0001) differedsignificantly among habitats Bonferroni comparisonsindicated that C morio Mi australis and Vespadelusspp were significantly more active in forest than in saltmarsh(P= 005 P = 0011 Plt 0001 Fig 3a b e) and urban habitats(P= 0002P= 0001P lt 0001 Fig 3ab e)Tadarida australiswas significantly more active in saltmarsh than in forest habitat(P= 0050 Fig 3d) whereas Mo sp 2 was significantly moreactive in saltmarsh (P lt 0001) andurban (P= 0001)habitats thanin the forest habitat (Fig 3c)

Although nightly bat activity did not differ among tidalcycles the activity of individual species did with significantlygreater activity recorded forMo sp 2 (F = 6339 P = 0018) andT australis (F= 5068 P = 0033) during neap tides (Fig 4a b)

Bat foraging activity

In all 268 feeding buzzes (17 of all calls) were recordedacross all habitats with 55 8 and 205 buzzes detected insaltmarsh urban and forest habitats respectively Proportionalfeeding activity differed significantly among habitats (df = 2c2 = 33600 Plt 0001) representing 40 04 and 16 ofcalls recorded in saltmarsh urban and forest habitatsrespectively Although the number of feeding buzzes recordedduring neap tides (159) was greater than spring tides (109)proportional feeding activity did not differ between the tidalcycles

Feeding buzzes were recorded for three species (C gouldii ndash15 Mi australis ndash 3 Mo sp 2 ndash 9) and one species group

14C morio

T australis Vespadelus spp

Mi australisMo sp 2

12(a)

(d ) (e)

(b) (c)

10

08

06

04

02 a a

a

aa

ab

b

b

aa

a

a

b b

b

00

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pass

es n

ight

ndash1)

plusmn S

E 08

20

15

10

05

00

10

06

04

02

00

08

10

12 6

5

4

3

2

1

0

06

04

02

00Saltmarsh Urban UrbanForest ForestSaltmarsh

Urban ForestSaltmarsh

Fig 3 Mean nightly bat activity in each habitat (a) Chalinolobus morio (b) Miniopterus australis (c) Mormopterus sp 2 (d) Tadarida australis(e) Vespadelus spp Means denoted by different letters are significantly different from one another

6

5

4

3

2

1

0Saltmarsh

Nig

htly

bat

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

aa

b

Urban Forest

Fig 2 Nightly bat activity recorded in each habitat Means denoted bydifferent letters are significantly different from one another

Do mosquitoes influence bat activity Wildlife Research 15

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

(Vespadelus spp ndash 241) Proportional feeding activity ofC gouldii and Vespadelus spp was significantly differentamong habitats (df = 2 c2 = 32976 P lt 0001 df = 2c2 = 6500 P = 0039) with most feeding activity beingrecorded in saltmarsh (313 and 1019) followed by urban(047 and 388) and forest (046 and 225) habitatsProportional feeding activity of all taxa combined did notdiffer between tidal cycles irrespective of habitat

Mosquito fauna

In all 70 364 mosquitoes were sampled across all habitatsduring the study representing 27 species (Table 2) The foresthabitat supported 25 species whereas 16 species and 14 specieswere present in saltmarsh and urban habitats respectively(Table 2) In all 33 125 (469) 3560 (51) and 33 679(479) mosquitoes were recorded in saltmarsh urban andforest habitats respectively

Aedes vigilax was the most abundant species in each habitatrepresenting 916 416 and 911 of all individualstrapped in saltmarsh urban and forest habitats respectively(Table 2) The other commonly collected species wereAe alternans and Cx sitiens being two species closelyassociated with estuarine habitats common banded mosquito(Cx annulirostris Skuse) being a species closely associated withfreshwater habitats and Cx molestus being a species associatedwith waste-water habitats (Table 2)

Whereas the abundance of Ae vigilax differed amonghabitats (H= 23966 Plt 0001 Fig 5) there was nosignificant difference between the tidal cycles (H= 0142P = 0706) Bonferroni comparisons revealed that Ae vigilaxabundance was significantly lower in urban habitat than insaltmarsh (P = 0001) and forest (P lt 0001) habitats

Non-mosquito fauna

Over 45 000 insects were sampled across all habitats duringthe study with 276 295 and 429 of all insectscollected in saltmarsh urban and forest habitats respectivelyMore than half of all sampled insects (677) were trappedduring neap tides Lepidopterans coleopterans dipterans andlsquootherrsquo insects (Blattodea Hemiptera Hymenoptera IsopteraOdonata and Orthoptera) represented 249 117 185and 457 of the sampled insects respectively

The abundance of all insects (all taxa pooled together) inthe lt5-mm size class was significantly different among habitats(F = 11394 P= 0001) with fewer of these insects being

recorded in urban habitat than in saltmarsh (P= 0015) andforest (P = 0001) habitats (Table 3) The abundance of allinsects in the 10ndash14-mm size class was also significantlydifferent among habitats (F= 9490 P = 0001) with greaterabundances recorded in forest habitat than in saltmarsh(P = 0002) and urban (P = 0005) habitats (Table 3) Theabundances of all insects in the 5ndash9-mm (F = 4215 P = 0043)and gt14-mm (F = 5049 P = 0030) size classes also differedamong habitats with greater abundances recorded in theforest habitat than in the saltmarsh habitat (P= 0044P = 0036 respectively for the two size classes) (Table 3) Theabundance of all insects (all size classes of all taxa pooledtogether) differed significantly among habitats (F = 9126P = 0003) with greater abundances recorded in forest than inurban habitat (P = 0003) (Table 3)

The abundances of certain insect taxa of a particular sizeclass also were found to differ among habitats Although theabundance of lepidopterans in the lt5-mm size class was foundto differ among habitats (F= 4090 P= 0034) pairwisecomparisons revealed that no single habitat differed fromanother A significant difference among habitats was observedfor the abundance of coleopterans in the 5ndash9-mm size class(F = 7996 P= 0004) with higher abundances recorded in theforest (P= 0006) and urban (P = 0014) habitats than in thesaltmarsh habitat (Table 3) The abundance of dipterans inthe lt5-mm size class was also significantly different amonghabitats (c2 = 16466 P = 0001) with significantly higherabundances in saltmarsh than in urban habitat (P = 0001)(Table 3) The abundance of other insects in the 10ndash14-mmsize class was found to differ among habitats (c2 = 10668P = 0005) with greater abundances recorded in the foresthabitat than in the saltmarsh (P = 0032) and urban (P = 0009)habitats (Table 3)

A significant interaction effect was observed for theabundance of all dipterans (all size classes pooled) (F = 3655P = 0047) with significantly more dipterans in the saltmarshhabitat during neap tides (Fig 6)

The abundances of all insects in the lt5-mm size class andall insects (all size classes of all taxa pooled together) weresignificantly greater during neap tides (F= 5233 P= 0038F = 5717 P = 0031 Table 3)

Relationships between bat activity and the abundanceof mosquito and non-mosquito prey

Relationships between response variables (nightly bat activityand the activity of individual species) and predictor variableswere not consistent across habitats In saltmarsh the abundanceof lepidopterans dipterans and all insects lt5mm in sizetogether accounted for 900 of the variability in nightly batactivity (df = 3 F= 4320 Plt 0001 Table 4) The abundanceof lepidopterans was positively correlated with the activity ofC gouldii (df = 1 R2 = 0306 F = 573 P= 0032 Table 4)The activity of Mo sp 2 was positively correlated withnightly insect abundance (df = 1 R2 = 0520 F = 1408P = 0002 Table 4) Vespadelus spp activity was positivelycorrelated with the abundances of coleopterans large insects(gt14mm) and Ae vigilax (df = 1 R2 = 0882 F = 3598P lt 0001 Table 4)

16 12

10

08

06

04

02

00

14

12

10

08

Nig

htly

act

ivity

ln (

x +

1)

(no

bat

pas

ses

nigh

tndash1)

plusmn S

E

06

04

02

00Neap Spring Neap Spring

(a) Mo sp 2 T australis(b)

Fig 4 Mean nightly bat activity during neap and spring tides(a) Mormopterus sp 2 (b) Tadarida australis

16 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

Tab

le2

Meansenigh

tlyab

unda

nceof

mosqu

itotaxa

ineach

habitatdu

ring

neap

andspring

tides

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Aedes

albo

annulatus

02plusmn08

02plusmn08

02plusmn05

07plusmn03

05plusmn03

06plusmn02

Aealternan

s12

0plusmn47

59plusmn29

88plusmn27

09plusmn06

02plusmn02

06plusmn03

26plusmn27

05plusmn04

15plusmn10

52plusmn19

23plusmn17

36plusmn18

Aeau

stralis

02plusmn02

01plusmn01

03plusmn02

05plusmn03

02plusmn10

09plusmn07

02plusmn01

05plusmn03

Aecamptorhynchu

s03plusmn03

10plusmn10

03plusmn03

01plusmn01

02plusmn02

07plusmn06

Aeflavifron

s03plusmn03

04plusmn04

02plusmn02

07plusmn07

01plusmn01

07plusmn06

Aemallochi

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aemultip

lex

01plusmn08

04plusmn03

03plusmn02

01plusmn08

08plusmn04

05plusmn02

13plusmn18

78plusmn52

47plusmn29

05plusmn04

39plusmn19

18plusmn10

Aeno

toscriptus

02plusmn08

03plusmn01

02plusmn07

49plusmn23

24plusmn12

35plusmn13

14plusmn03

10plusmn02

11plusmn02

22plusmn08

12plusmn04

16plusmn05

Aepa

lmarum

00plusmn00

01plusmn06

02plusmn02

02plusmn10

04plusmn02

07plusmn06

06plusmn03

Aeprocax

02plusmn02

01plusmn02

02plusmn02

01plusmn10

14plusmn07

120plusmn92

70plusmn49

05plusmn03

41plusmn31

24plusmn17

Aequ

asirub

rithorax

03plusmn03

02plusmn02

01plusmn01

07plusmn07

06plusmn06

03plusmn03

Aerubrith

orax

03plusmn03

04plusmn03

03plusmn02

09plusmn08

01plusmn09

02plusmn06

Aetrem

ulus

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Aevigilax

5282plusmn34

79

2611plusmn12

75

3868plusmn17

42

134plusmn50

159plusmn76

147plusmn45

3394plusmn11

38

32930plusmn13

43

3340plusmn86

329

36plusmn12

48

2021plusmn65

024

52plusmn67

6Anoph

eles

annulip

es04plusmn03

06plusmn04

05plusmn02

01plusmn01

06plusmn03

08plusmn06

05plusmn04

04plusmn02

04plusmn02

An

atratip

es02plusmn02

10plusmn10

06plusmn06

03plusmn03

Coquillettidialin

ealis

05plusmn03

02plusmn02

03plusmn02

03plusmn03

10plusmn10

08plusmn04

01plusmn06

04plusmn02

03plusmn02

05plusmn02

02plusmn07

Culex

annulirostris

14plusmn05

26plusmn12

23plusmn07

02plusmn09

06plusmn04

05plusmn02

92plusmn76

87plusmn46

86plusmn42

36plusmn26

38plusmn16

37plusmn15

Cxau

stralicus

04plusmn03

02plusmn02

04plusmn03

02plusmn02

01plusmn06

01plusmn08

01plusmn08

01plusmn05

05plusmn03

02plusmn02

02plusmn06

Cxmolestus

02plusmn08

04plusmn01

03plusmn08

33plusmn17

186plusmn99

114plusmn55

04plusmn02

06plusmn02

05plusmn02

13plusmn07

65plusmn36

46plusmn19

Cxorbostiensis

05plusmn03

02plusmn02

03plusmn02

01plusmn01

09plusmn04

01plusmn06

08plusmn08

01plusmn06

01plusmn06

09plusmn05

09plusmn03

09plusmn03

Cxqinquefasciatus

08plusmn02

09plusmn01

08plusmn01

33plusmn18

32plusmn13

33plusmn07

08plusmn02

06plusmn03

07plusmn02

17plusmn04

16plusmn04

16plusmn03

Cxsitiens

47plusmn34

247plusmn11

315

4plusmn65

02plusmn01

16plusmn10

09plusmn05

05plusmn05

08plusmn05

07plusmn03

18plusmn17

96plusmn42

56plusmn23

Mansoniaun

iform

is02plusmn02

10plusmn10

06plusmn06

03plusmn03

Tripteroidesatripes

03plusmn03

10plusmn10

07plusmn07

03plusmn03

Verrallina

funerea

03plusmn03

01plusmn01

08plusmn08

04plusmn04

VeENM

arks

No

5203plusmn03

01plusmn10

08plusmn07

04plusmn03

Total

3965plusmn22

00

3004plusmn13

91

3456plusmn12

34

269plusmn63

440plusmn17

536

0plusmn97

3404plusmn11

40

3629plusmn13

63

3523plusmn87

225

46plusmn85

923

58plusmn68

224

46plusmn53

7

Do mosquitoes influence bat activity Wildlife Research 17

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

In theurbanhabitat the activityofMiaustraliswasnegativelycorrelated with the abundance of lsquootherrsquo insects and positivelycorrelated with the abundance of dipterans (df = 2 R2 = 0319F = 451 P = 0033 Table 4) A significant relationship betweenprey-abundance variables and the activity of bats was observedfor Vespadelus spp with activity being positively correlatedwith the abundance of dipterans (df = 1 R2 = 0413 F = 984P = 0007 Table 4)

In the forest habitat activity of C gouldii was negativelycorrelated with dipteran abundance (df = 1 R2 = 0318F = 705 P= 0021 Table 4) The activity of Vespadelusspp was positively correlated with the abundance of Aevigilax (df = 1 R2 = 0511 F = 1566 P= 0001 Table 4)

Discussion

The present study is the first to comprehensively investigaterelationships between bat activity and mosquito prey as wellas other insects across a range of coastal habitats Complexspatial and temporal relationships exist among bats prey and thelocal environment Although prey (Ae vigilax and all non-mosquito prey) were generally most abundant in saltmarsh andforest habitats relationships between prey abundances and totalbat activity were only identified in the less-cluttered saltmarshhabitat Additionally proportional feeding activity was greatestin saltmarsh However relationships between prey abundanceand the activity of particular specieswere identified in all habitatsOnly the activity of bats of the Vespadelus genus was positivelycorrelatedwithAe vigilax abundance in both saltmarsh and foresthabitats suggesting that Ae vigilax may be an important preyresource for these bats which is consistent with concurrentdetailed dietary investigations (Gonsalves 2012)

Bat commuting and feeding activity

Activity of individual species differed among habitatshowever these differences can be explained by species-specific echolocation design and wing morphologyChalinolobus morio Mi australis and Vespadelus spp weresignificantly more active in the forest These three taxa employ

high-frequency echolocation considered to be appropriate forforaging close to edges of cluttered environments Activity ofMo sp 2 was significantly higher in saltmarsh and urbanhabitats than in forest habitat whereas activity of T australiswas significantly greater in saltmarsh than in forest habitat It ispossible that calls from the high-flyingT australismayhave beenattenuated by vegetation in the forest canopy deflating the actuallevel of activity of this bat However bothT australis andMo sp2 are clutter-sensitive fast-flying bats that are adapted to foragingin more open areas (Fullard et al 1991 Law and Chidel 2002Adams et al 2009) Both Mo sp 2 and T australis weresignificantly more active during neap tides It is possible thatthese two species weremitigating the risk of predation associatedwith foraging in open habitats (Speakman 1991 Baxter et al2006) during periods of greater lunar illumination (spring tides)However we did not observe any nocturnal predators (ie owls)during the study (L Gonsalves pers obs)

Total nightly bat activity was significantly higher in forestsupporting the findings of previous studies comparing forestedand urban habitats (Legakis et al 2000 Avila-Flores and Fenton2005 Hourigan et al 2006) However other studies have failedto detect significant differences among landscape categories(eg urban v vegetated) but have detected significantdifferences among landscape elements within these categories(eg bushland v backyard Threlfall et al 2011) In other studieswetlands have been found to be productive habitats for bats withsignificantly greater bat activity recorded in this habitat than inadjacent upland forested areas (Brosset et al 1995 Menzel et al2005) Although bat activity was significantly higher in the foresthabitat the proportion of activity that represented feeding wassignificantly greater in saltmarsh Studies have suggested thatsaltmarsh may be productive for foraging bats given that insectsform a major component of terrestrial fauna within the habitat(Laegdsgaard et al 2004) Although neighbouring habitats suchasmangrove forests are known to be productive foraging habitatsfor bats elsewhere (McKenzie and Rolfe 1986 Hoye 2002) wefound that insect numbers were highly variable and generallysimilar between forest and saltmarsh (see below) Fenton (1990)suggested that itmaybeenergetically less demandingandperhapsmore efficient to locate prey in an open habitat such as saltmarshthan in a cluttered forest environment and this hypothesismay serve as a reasonable explanation for the discrepancy inproportional feeding activity detected between saltmarsh andforest habitats particularly because the overall abundances ofprey (mosquito and non-mosquito) were similar in both habitats

The proportional feeding activity of two bat taxa (C gouldiiand Vespadelus spp) was also significantly higher in the moreopen saltmarsh habitat than the urban and forest habitatsAlthough similar levels of overall activity were detected forC gouldii in each habitat the higher level of feeding activityin the more open saltmarsh may reflect the influence of clutter onthe foraging activity of this bat species C gouldii is an edge-adapted clutter-sensitive bat species (Fullard et al 1991LawandChidel 2002 Adams et al 2009) capable of foraging in openspaces and edge environments Although C gouldiimay be ableto negotiate openings in forest habitats foraging (involvingdetection pursuit and capture of prey as well as collisionavoidance) is likely to be more difficult in the cluttered foresthabitat than in the more open saltmarsh habitat Vespadelus spp

6

5 a

b

a

4

3

2

1

0

Nig

htly

Aed

es v

igila

x ab

unda

nce

ln (

x +

1)

plusmn S

E

Urban ForestSaltmarsh

Fig 5 Mean nightly Aedes vigilax abundance recorded in each habitatMeansdenotedbydifferent letters are significantly different fromone another

18 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

Tab

le3

Meansenigh

tlyab

unda

nces

ofinsect

taxa

andinsect

size

classesin

each

habitatdu

ring

neap

andspring

tides

Means

follo

wed

bydifferentletters(low

ercase

forhabitatsandup

percase

forneap

andspring

tides)with

inthesamerowaresign

ificantly

differentfrom

oneanother

Taxon

Saltm

arsh

Urban

Forest

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Neap

Spring

Total

Lepidop

tera

lt5mm

525plusmn11

529

9plusmn10

240

5plusmn80

474plusmn10

122

2plusmn50

333plusmn60

2003plusmn62

720

03plusmn64

720

03plusmn47

383

4plusmn20

486

2plusmn27

485

1plusmn18

05ndash9mm

135plusmn42

137plusmn52

136plusmn33

220plusmn70

136plusmn27

173plusmn35

545plusmn17

730

6plusmn86

379plusmn83

259plusmn60

195plusmn37

221plusmn33

10ndash14

mm

68plusmn36

16plusmn06

40plusmn18

84plusmn54

21plusmn07

49plusmn24

160plusmn90

89plusmn21

111plusmn30

95plusmn31

43plusmn10

64plusmn14

gt14mm

12plusmn08

04plusmn02

07plusmn04

27plusmn13

03plusmn02

14plusmn06

35plusmn13

37plusmn13

36plusmn10

23plusmn07

15plusmn06

18plusmn04

Allsizes

740plusmn16

745

6plusmn10

858

8plusmn10

180

6plusmn20

837

7plusmn68

565plusmn10

927

40plusmn80

924

30plusmn73

325

25plusmn54

712

10plusmn27

311

12plusmn31

311

52plusmn21

4Coleoptera

lt5mm

579plusmn44

515

9plusmn68

355plusmn21

033

3plusmn11

214

7plusmn65

228plusmn63

943plusmn49

452

0plusmn20

065

0plusmn20

156

4plusmn20

428

0plusmn81

396plusmn97

5ndash9mm

33plusmn22

05plusmn04

18a

plusmn11

194plusmn72

54plusmn15

116bplusmn36

408plusmn22

519

1plusmn74

258bplusmn85

179plusmn63

86plusmn30

124plusmn31

10ndash14

mm

01plusmn01

06plusmn05

04plusmn03

23plusmn10

10plusmn04

16plusmn05

120plusmn94

41plusmn19

65plusmn31

36plusmn22

20plusmn07

26plusmn10

gt14mm

06plusmn03

00plusmn00

03plusmn02

01plusmn01

03plusmn02

03plusmn01

13plusmn08

24plusmn15

21plusmn11

06plusmn02

10plusmn05

08plusmn03

Allsizes

618plusmn46

717

0plusmn70

379plusmn22

055

1plusmn17

121

1plusmn83

360plusmn95

1482plusmn81

977

3plusmn30

299

1plusmn32

078

4plusmn26

239

3plusmn12

055

3plusmn13

0Diptera

lt5mm

3376plusmn14

23

652plusmn12

519

23a

plusmn73

526

4plusmn10

323

7plusmn51

249bplusmn51

878plusmn29

382

0plusmn25

283

8ab

plusmn19

016

11plusmn63

456

7plusmn10

699

4plusmn27

45ndash9mm

107plusmn44

38plusmn12

71plusmn23

49plusmn27

11plusmn06

28plusmn13

45plusmn19

179plusmn14

413

8plusmn10

071plusmn21

78plusmn50

75plusmn31

10ndash14

mm

25plusmn22

00plusmn00

11plusmn10

00plusmn00

01plusmn01

01plusmn01

08plusmn05

09plusmn07

08plusmn05

11plusmn09

03plusmn02

07plusmn04

gt14mm

01plusmn01

00plusmn00

00plusmn00

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn01

00plusmn00

01plusmn01

01plusmn00

Allsizes

3509plusmn14

30

690plusmn13

020

06plusmn74

531

3plusmn10

824

7plusmn51

276plusmn54

927plusmn29

210

06plusmn23

698

2plusmn18

016

92plusmn64

264

6plusmn10

910

74plusmn27

7lsquoO

therrsquo

lt5mm

150plusmn84

96plusmn49

121plusmn46

106plusmn53

67plusmn26

84plusmn27

225plusmn77

258plusmn10

524

8plusmn74

149plusmn41

142plusmn42

145plusmn30

5ndash9mm

18plusmn09

15plusmn04

16plusmn05

10plusmn08

27plusmn12

19plusmn08

75plusmn50

51plusmn21

58plusmn20

27plusmn13

32plusmn09

30plusmn07

10ndash14

mm

03plusmn03

02plusmn01

03a

plusmn01

11plusmn06

01plusmn01

06a

plusmn03

38plusmn18

37plusmn14

37b

plusmn11

14plusmn05

14plusmn06

14plusmn04

gt14mm

09plusmn07

02plusmn01

05plusmn03

09plusmn06

02plusmn01

05plusmn03

38plusmn23

12plusmn05

20plusmn08

15plusmn06

06plusmn02

09plusmn03

Allsizes

179plusmn85

115plusmn49

145plusmn46

135plusmn59

94plusmn32

112plusmn31

373plusmn16

135

7plusmn11

036

2plusmn87

205plusmn55

191plusmn47

197plusmn35

Allinsects

lt5mm

4629plusmn12

66

1207plusmn25

428

04a

plusmn73

911

77plusmn27

066

9plusmn17

289

2bplusmn16

144

37plusmn97

336

00plusmn88

238

99a

plusmn65

133

07A

plusmn63

918

49B

plusmn40

224

65plusmn36

85ndash9mm

292plusmn83

195plusmn56

241aplusmn49a

473plusmn15

522

1plusmn39

331ab

plusmn76

1015plusmn35

472

1plusmn25

582

6bplusmn20

354

9plusmn12

638

6plusmn10

045

5plusmn79

10ndash14

mm

97plusmn38

24plusmn06

58a

plusmn20a

119plusmn57

29plusmn08

68a

plusmn27

301plusmn14

917

3plusmn40

219bplusmn58

159plusmn48

77plusmn20

112plusmn24

gt14mm

27plusmn12

06plusmn02

16a

plusmn06a

36plusmn12

09plusmn03

21abplusmn06

79plusmn26

72plusmn28

74b

plusmn20

44plusmn10

30plusmn11

36plusmn08

Allsizes

5046plusmn12

44

1431plusmn27

331

18abplusmn74

918

05plusmn42

292

9plusmn20

513

12b

plusmn23

758

32plusmn13

44

4565plusmn10

99

5018a

plusmn83

940

59A

plusmn69

823

42B

plusmn50

130

67plusmn42

8

Do mosquitoes influence bat activity Wildlife Research 19

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

however are agile bats adapted to fly close to edges of clutteredvegetation (OrsquoNeill and Taylor 1986 Rhodes 2002) Althoughthese bats were significantly more active in forest greaterproportional feeding activity by these taxa was recorded insaltmarsh Clutter-tolerant bats are known to forage in less-cluttered habitats when prey abundances are high (Pavey et al2001) Radio-tracking of V vulturnus in the study area alsoindicated that this species spent proportionately more time inforest than in saltmarsh (Gonsalves 2012) However it shouldbe noted that saltmarsh constitutes a very small proportion(18 ha) of the total habitat available to bats in the study area

Prey abundance

Aedes vigilax was the most abundant mosquito species in eachhabitat However the abundance of Ae vigilax was significantlyhigher in saltmarsh and forest habitats than in the urbanhabitat Saltmarsh habitat represents a major larval habitat ofAe vigilax supporting abundant populations of adult Ae vigilaxparticularly in the days immediately following emergence fromtheir immature stages Forest habitat is likely to provide adultAe vigilax populations a humid refuge and sources of blood

meals sustaining population abundances for longer periods thando exposed saltmarsh environments

Nightly abundance of each insect taxon across differenthabitats decreased with body size a phenomenon reported in astudy investigating relationships between arthropod abundanceand body size in an Indonesian rainforest (Stork and Blackburn1993) In our study average nightly insect abundance in foresthabitat was 38 times greater than insect abundance recordedin the urban habitat Whereas this trend has been observedpreviously in some studies (Avila-Flores and Fenton 2005)other studies have found that suburban habitats with sandstonegeology support similar levels of insect biomass as do bushlandhabitats of the same geology (Threlfall et al 2011) Given thegeology of our study area is dominated byHawkesbury sandstonethat overlies Narrabeen shales and sandstone (NSW NationalParks and Wildlife Service 1999) it is unclear why the foresthabitat supported greater abundances of insects than did the urbanhabitat

Nightly insect abundance was not consistent among habitatsand tidal cycle for all taxa and all size classes of insectsGenerallysmall insects (lt5mm) were similarly abundant in saltmarsh andforest habitats and were significantly less abundant in urbanhabitats whereas large insects (10mm)were significantlymoreabundant in the forest habitat In the present study nightly insectabundance and the abundance of small insects (lt5mm) weresignificantly greater during neap tides Because tidal and lunarcycles are related it is difficult to identify whether the observeddifference in insect abundance was due to the tide lunarillumination or both

Relationships between prey abundance and bat activity

In the present study failure to detect a relationship betweenAe vigilax abundance and nightly bat activity (all bat speciespooled together) in any of the habitats investigated was notunexpected given Ae vigilax is not likely to be available to allbat species because of constraints imposed on prey detectabilityby echolocation frequency (Moslashhl 1988 Barclay and Brigham1991) However activity of Vespadelus spp was positively

7

6

5

4

3

2

Nig

htly

abu

ndan

ce ln

(x

+ 1

) plusmn

SE

1

0Saltmarsh Urban

Diptera (all sizes)

Neap Spring

Forest

Fig 6 Nightly abundanceof dipterans (all sizes) in each habitat during neapand spring tides Asterisk denotes significant interaction effect

Table 4 Final statistical models for relationships between prey variables and bat activity in each habitat based on Akaike information criterion(AICc) score (corrected for small sample size) ranking of models

Lep = all lepidopterans Col = all coleopterans Dip = all dipterans Other = all other insects lt5mm= all insects lt5 mm gt14mm= all insects gt14mm

Habitat Species AICc Variables Coefficient T P Modelin model R2 F P

Saltmarsh Nightly activity ndash115347 Lep 025990 251 0029 0900 4320 lt0001Dip ndash085650 ndash568 lt0001

lt5mm 127240 715 lt0001Chalinolobus gouldii ndash457533 Lep 050590 239 0032 0306 573 0032Mormopterus sp 2 ndash548820 All 044260 375 0002 0520 1408 0002Vespadelus spp ndash111306 Ae vigilax 020474 346 0005 0882 3598 lt0001

Col 069998 834 lt0001gt14mm 059770 365 0004

Urban Miniopterus australis ndash223056 Dip 015644 250 0027 0319 451 0033Other ndash011871 ndash256 0024

Vespadelus spp ndash496057 Dip 045730 314 0007 0413 984 0007Forest Chalinolobus gouldii ndash465227 Dip ndash06466 ndash265 0021 0318 705 0021

Vespadelus spp ndash545900 Ae vigilax 072090 396 0001 0511 1566 0001

20 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

correlated with Ae vigilax abundance Members of this genusutilise high-frequency echolocation considered to be suited todetection of small-sized prey such as mosquitoes (Barclay andBrigham 1991) Additionally members of this genus are smallin size (V vulturnus 4 g V pumilus 45 g) a characteristicassociated with consumption of small-sized prey givenconstraints imposed by morphology (eg jaw structure) Givenlow sample sizes of many bat taxa considered capable ofdetecting small prey such as Ae vigilax (high-frequencyecholocating bats) it was not possible to examine relationshipsbetween Ae vigilax abundance and activity of these bat taxa Norelationship was observed between Ae vigilax abundance andthe activity of Mi australis Although Ae vigilax representsan abundant prey resource for this small-sized speciesincreased energetic requirements of this bat (compared withsmaller bats of the Vespadelus genus) in association with thelower profitability of mosquitoes (206 kJ gndash1 ndash Cummins andWuycheck 1971 Kunz 1988) than other abundant prey taxa(eg moths 272 kJ gndash1 ndash McLean and Speakman 1999beetles 2448 kJ gndash1 ndash Cummins and Wuycheck 1971 Kunz1988) may diminish the importance of Ae vigilax as a preyresource to this larger bat species

Many studies have found bat activity to be positivelycorrelated with the abundance of insects (de Jong and Ahleacuten1991 OrsquoDonnell 2000 Adams et al 2009) In the presentstudy bat activity tended to be positively correlated with preyabundance although relationships varied among habitatsAbundances of lepidopterans dipterans and insects lt5mmtogether were significant predictors of nightly bat activity inthe saltmarsh habitat accounting for 900 of variabilityobserved in this habitat Studies investigating the influence ofvegetation clutter on access to prey by bats have demonstratedthat prey abundance does not necessarily equate to preyavailability (Boonman et al 1998 Adams et al 2009 Rainhoet al 2010) In the present study failure to detect any significantrelationships between prey abundance and overall bat activityin the urban and forest habitats may reflect a negative influenceof clutter on prey detectability or the activity of clutter-sensitivespecies Although no direct measurements of clutter were madeduring the present study it is likely that forest (with understoreymid-storey and canopy) and urban habitats (with retained naturaland domestic vegetation aswell as urban structures eg telegraphpoles) were acoustically and physically more complex than thegenerally very open saltmarsh habitat However it should beacknowledged that the patchy distribution of juvenile mangroves(height lt3m) transgressing into saltmarsh habitat is likely togenerate moderate levels of clutter that may have an impacton low-flying foraging bats in saltmarsh habitat Additionallyclimatic variables are known to influence bat and insectpopulations (Taylor 1963 Lacki 1984 Negraeff and Brigham1995 OrsquoDonnell 2000) In the present study climatic variablessuch as temperature and humidity were not measured althoughsurveys were undertaken only during conditions consideredsuitable for bats ie we did not sample during heavy rainfall

Given most insects in each habitat were small (lt5mm) it wasexpected that positive relationships between prey abundance andactivity of clutter-sensitive batsweremore likely to be detected inthe more open (less cluttered) saltmarsh habitat In the presentstudy positive relationships betweenpreyabundance andactivity

of bats were observed in saltmarsh for three taxa (C gouldiiMo sp 2 and Vespadelus spp) Two of these taxa are clutter-sensitive low-frequency echolocating bats (Fullard et al1991) C gouldii was positively correlated with the abundanceof lepidopterans whereas Mo sp 2 was positively correlatedwith nightly insect abundance Given small prey (2ndash10mm)have been identified as a dominant size class in the diets ofboth C gouldii and Mo sp 2 in other areas (unpubl data ofLumsden and Wainer in Lumsden 2004) it is not surprisingthat the activity levels of C gouldii and Mo sp 2 werepositively correlated with abundance of small prey but notlarger prey

The strongest positive relationship between prey abundanceand bat activity in the more open saltmarsh habitat was observedfor Vespadelus spp Although the bats that make up this speciesgroup are small agile bats that utilise high-frequencyecholocation (gt50 kHz) suited to flying close to edges of high-clutter vegetation they are not restricted to foraging in clutteredhabitatsColeopteran abundance explainedmost of the variabilityin the activity of these taxa whereas large insects (gt14mm) andthe abundance of Ae vigilax accounted for a smaller amountof the variability Given morphological constraints on thesetaxa associated with jaw size and prey hardness (Freeman andLemen 2007) it is unlikely that the relationship betweenVespadelus spp activity and large insects (gt14mm) reflects anecological response of Vespadelus spp to the abundance of thisprey resource The positive relationship between coleopteranabundance (dominated by small beetles lt5mm) and theabundance of Ae vigilax (typically lt5mm) with the activity ofVespadelus spp is more likely to reflect an ecologically relevantresponse

Positive relationships between prey abundance and theactivity of clutter-sensitive bats (C gouldii and Vespadelusspp) in the more cluttered forest habitat also were identifiedC gouldii uses broadband frequency-modulated quasi-constantfrequency (FM-QCF) echolocation calls typical of edge-space foraging bats (Adams et al 2009) Additionally the useof alternating frequencies in successive pulses may allow fordetection of near targets in a cluttered forest (Jones and Corben1993) Vespadelus spp are suited to foraging close to the edgesof cluttered vegetation as well as detecting small prey such asmosquitoes While it is not surprising that a strong positiverelationship was observed between the activity of this speciesgroup and the abundance of Ae vigilax small lepidopterans(lt5mm) were also abundant in the forest habitat yet did notaccount significantly for variability in the activity of thisbat species group One possible explanation for this may bethe lower profitability of tympanate moths which are able todetect and avoid echolocating bats making their capture bybats more difficult than for other non-tympanate taxa

While prey (Ae vigilax and all non-mosquito prey) weregenerally most abundant in saltmarsh and forest habitatspositive associations between total bat activity and preyabundance as well as greater proportional feeding activityoccurred in the less cluttered saltmarsh habitat The abundanceof Ae vigilax was positively correlated with the activity of batsof the Vespadelus genus supporting the view that Ae vigilaxmay be an important prey resource for these bats Togetherthese findings suggest that open habitats that occur in close

Do mosquitoes influence bat activity Wildlife Research 21

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

juxtaposition to forested habitats providing roosts are likely to beprofitable foraging areas for bats

Acknowledgements

This researchwas funded by theNSWEnvironmental Trust (2007RD0071)We thank N Saintilan for his contribution to the design of the study Wethank the volunteers who assisted in the field and R De Geer and S Silwalfor assistance with insect sorting We also thank J Clancy for assistance withmosquito identification

References

Adams M D Law B S and French K O (2009) Vegetation structureinfluences the vertical stratification of open- and edge-space aerial-foraging bats in harvested forests Forest Ecology and Management258 2090ndash2100 doi101016jforeco200908002

Adams M D Law B S and Gibson M S (2010) Reliable automation ofbat call identification for eastern New South Wales Australia usingclassification trees and AnaScheme software Acta Chiropterologica 12231ndash245 doi103161150811010X504725

Avila-Flores R and FentonMB (2005)Use of spatial features by foraginginsectivorous bats in a large urban landscape Journal of Mammalogy 861193ndash1204 doi10164404-MAMM-A-085R11

Barclay R M R and Brigham R M (1991) Prey detection dietary nichebreadth and body size in bats why are aerial insectivorous bats so smallAmerican Naturalist 137 693ndash703 doi101086285188

BaxterD JMPsyllakis JMGillinghamMP andOrsquoBrienEL (2006)Behavioural response of bats to perceived predation risk while foragingEthology 112 977ndash983 doi101111j1439-0310200601249x

Belbaseacute S (2005) Presence and activity of insectivorous bats in saltmarshhabitat at KooragangNature Reserve Newcastle BSc(Honours) ThesisAustralian Catholic University Sydney

Bell G P (1980) Habitat use and response to patches of prey by desertinsectivorous bats Canadian Journal of Zoology 58 1876ndash1883doi101139z80-256

Bell KM (1989) Development and review of the contiguous local authoritygroup programme on saltmarsh mosquito control Arbovirus Research inAustralia 5 168ndash171

Bell S A J (2009) The natural vegetation of the Gosford local governmentarea Central Coast New South Wales vegetation community profilesEast Coast Flora Survey Unpublished Report to Gosford City CouncilNovember 2009 Gosford NSW

Boonman A M Boonman M Bretschneider F and van de Grind W A(1998) Prey detection in trawling insectivorous bats duckweedaffects hunting behaviour in Daubentonrsquos bat Myotis daubentoniiBehavioral Ecology and Sociobiology 44 99ndash107 doi101007s002650050521

Bradshaw P (1996) The physical nature of vertical forest habitat and itsimportance in shaping bat species assemblages In lsquoBats and ForestsSymposiumrsquo (Eds R M R Barclay and R M Brigham) pp 199ndash212(British Columbia Ministry of Forests Victoria Canada)

Brigham R M Grindal S D Firman M C and Morissette J L (1997)The influenceof structural clutteronactivitypatternsof insectivorousbatsCanadian Journal of Zoology 75 131ndash136 doi101139z97-017

Brosset A Cosson J F Gaucher P and Masson P (1995) The batcommunity in a coastal marsh of French Guyana composition of thecommunity Mammalia 59 527ndash535

Cryan P M Bogan M A and Altenbach J S (2000) Effect of elevationon distribution of female bats in the Black Hills South Dakota Journalof Mammalogy 81 719ndash725 doi1016441545-1542(2000)081lt0719EOEODOgt23CO2

Cummins K W and Wuycheck J C (1971) Caloric equivalents forinvestigations in ecological energetics Mitteilung InternationaleVereinigung fuer Theoretische unde Amgewandte Limnologie 18 1ndash158

de Jong J and Ahleacuten I (1991) Factors affecting the distribution of bats inUppland central Sweden Holarctic Ecology 14 92ndash96

de Little S C Bowman D M J S Whelan P I Brook B W andBradshaw C J A (2009) Quantifying the drivers of larvaldensity patterns in two tropical mosquito species to maximize controlefficiency Environmental Entomology 38 1013ndash1021 doi1016030220380408

Fenton M B (1990) The foraging ecology and behavior of animal-eatingbats Canadian Journal of Zoology 68 411ndash422 doi101139z90-061

Fenton M B (1997) Science and the conservation of bats Journal ofMammalogy 78 1ndash14 doi1023071382633

FentonM B andMorris G K (1976) Opportunistic feeding by desert bats(Myotis spp) Canadian Journal of Zoology 54 526ndash530 doi101139z76-059

Freeman PW andLemenCA (2007) Using scissors to quantify hardnessof insects do bats select for size or hardness Journal of Zoology 271469ndash476 doi101111j1469-7998200600231x

Fukui D A I Murakami M Nakano S and Aoi T (2006) Effect ofemergent aquatic insects on bat foraging in a riparian forest Journal ofAnimal Ecology 75 1252ndash1258 doi101111j1365-2656200601146x

Fullard J Koehler C SurlykkeA andMcKenzieN (1991) Echolocationecology and flight morphology of insectivorous bats (Chiroptera) insouth-western Australia Australian Journal of Zoology 39 427ndash438doi101071ZO9910427

Gehrt S D and Chelsvig J E (2003) Bat activity in an urban landscapepatterns at the landscape and microhabitat scale Ecological Applications13 939ndash950 doi10189002-5188

Gibson M and Lumsden L (2003) The AnaScheme automated bat callidentification system Australasian Bat Society Newsletter 20 24ndash26

Gonsalves L (2012) Saltmarsh mosquitoes and insectivorous bats seekinga balance PhD Thesis Australian Catholic University Sydney

Gonsalves L Law BWebb C andMonamy V (in press) Are vegetationinterfaces important to foraging insectivorous bats in endangeredcoastal saltmarsh on the Central Coast of New South Wales PacificConservation Biology

Griffin D RWebster F A andMichael C R (1960) The echolocation offlying insects by bats Animal Behaviour 8 141ndash154 doi1010160003-3472(60)90022-1

Hourigan C Johnson C and Robson S (2006) The structure of a micro-bat community in relation to gradients of environmental variation in atropical urban area Urban Ecosystems 9 67ndash82 doi101007s11252-006-7902-4

Hourigan C L Catterall C P Jones D and Rhodes M (2010) Thediversity of insectivorous bat assemblages among habitats within asubtropical urban landscape Austral Ecology 35 849ndash857 doi101111j1442-9993200902086x

Hoye G (2002) Pilot survey for microchiropteran bats of the mangroveforest of Kooragang Island the Hunter Estuary New South WalesUnpublished report to Newcastle City Council NSW

Jones G (1999) Scaling of echolocation call parameters in bats The Journalof Experimental Biology 202 3359ndash3367

Jones G and Corben C (1993) Echolocation calls from six speciesof microchiropteran bats in southeastern Queensland AustralianMammalogy 16 35ndash38

Kokkinn M J Duval D J and Williams C R (2009) Modelling theecology of the coastal mosquitoes Aedes vigilax and Aedescamptorhynchus at Port Pirie South Australia Medical and VeterinaryEntomology 23 85ndash91 doi101111j1365-2915200800787x

Kuenzi A J andMorrisonM L (2003) Temporal patterns of bat activity insouthern Arizona The Journal of Wildlife Management 67 52ndash64doi1023073803061

Kunz T H (1988) Methods for assessing prey availability for insectivorousbats In lsquoEcological and Behavioral Methods for the Study of Batsrsquo(Ed THKunz) pp 191ndash210 (Smithsonian Institute PressWashingtonDC)

22 Wildlife Research L Gonsalves et al

Lacki M J (1984) Temperature and humidity-induced shifts in theflight activity of little brown bats The Ohio Journal of Science 84264ndash266

Laegdsgaard P Monamy V and Saintilan N (2004) Investigating thepresence of threatened insectivorous bats on coastal NSW saltmarshhabitat Wetlands (Australia) 22 29ndash41

Lamb S (2009) The importance of saltmarsh and estuarine macrohabitatfor insectivorous bats on the Central Coast NSW BSc(Honours)Thesis Australian Catholic University Sydney

Law B and Chidel M (2002) Tracks and riparian zones facilitate the useof Australian regrowth forest by insectivorous bats Journal of AppliedEcology 39 605ndash617 doi101046j1365-2664200200739x

Law B S and Lean M (1999) Common blossom bats (Syconycterisaustralis) as pollinators in fragmented Australian tropical rainforestBiological Conservation 91 201ndash212 doi101016S0006-3207(99)00078-6

Legakis A Papadimitriou C GaethlichM and Lazaris D (2000) Surveyof the bats of the Athens metropolitan area Myotis 38 41ndash46

Lloyd A Law B and Goldingay R (2006) Bat activity on riparianzones and upper slopes in Australian timber production forests and theeffectiveness of riparian buffers Biological Conservation 129 207ndash220doi101016jbiocon200510035

Lookingbill T R Elmore A J Engelhardt K A M Churchill J BEdward Gates J and Johnson J B (2010) Influence of wetlandnetworks on bat activity in mixed-use landscapes BiologicalConservation 143 974ndash983 doi101016jbiocon201001011

Lumsden L (2004) The ecology and conservation of insectivorous bats inrural landscapes PhD Thesis Deakin University Geelong Vic

Lumsden L F and Bennett A F (2005) Scattered trees in rural landscapesforaging habitat for insectivorous bats in south-eastern AustraliaBiological Conservation 122 205ndash222 doi101016jbiocon200407006

McKenzie N L and Rolfe J K (1986) Structure of bat guilds in theKimberley mangroves Australia Journal of Animal Ecology 55401ndash420 doi1023074727

McLean J A and Speakman J R (1999) Energy budgets of lactatingand non-reproductive brown long-eared bats (Plecotus auritus) suggestfemales use compensation in lactation Functional Ecology 13 360ndash372doi101046j1365-2435199900321x

Menzel J Menzel M Kilgo J Ford W and Edwards J (2005) Batresponse to Carolina bays and wetland restoration in the southeasternUS coastal plain Wetlands 25 542ndash550 doi1016720277-5212(2005)025[0542BRTCBA]20CO2

Moslashhl B (1988) Target detection by insectivorous bats In lsquoAnimalSonar Systems Processes and Performancersquo (Eds P E Natchigall andP W B Moore) pp 435ndash450 (Plenum Press New York)

Negraeff E and Brigham R M (1995) The influence of moonlight onthe activity of little brown bats (Myotis lucifugus) Zeitschrift furSaugetierkunde 60 330ndash336

Neuweiler G (1984) Foraging echolocation and audition in batsNaturwissenschaften 71 446ndash455 doi101007BF00455897

Norberg U M and Rayner J M V (1987) Ecological morphologyand flight in bats (Mammalia Chiroptera) wing adaptations flightperformance foraging strategy and echolocation PhilosophicalTransactions of the Royal Society of London Series B BiologicalSciences 316 335ndash427 doi101098rstb19870030

NSW National Parks and Wildlife Service (1999) Bouddi NationalPark Plan of Management NSW National Parks and Wildlife ServiceGosford

OrsquoDonnell C F J (2000) Influence of season habitat temperature andinvertebrate availability on nocturnal activity of the New Zealand long-tailed bat (Chalinolobus tuberculatus) New Zealand Journal of Zoology27 207ndash221 doi1010800301422320009518228

OrsquoDonnell C F J (2001) Home range and use of space by Chalinolobustuberculatus a temperate rainforest bat from New Zealand Journal ofZoology 253 253ndash264 doi101017S095283690100022X

OrsquoNeill M G and Taylor R J (1986) Observations on the flight patternsand foraging behaviour of Tasmanian bats Wildlife Research 13427ndash432 doi101071WR9860427

Pavey C Grunwald J-E and Neuweiler G (2001) Foraging habitat andecholocation behaviour of Schneiderrsquos leafnosed bat Hipposiderosspeoris in a vegetation mosaic in Sri Lanka Behavioral Ecology andSociobiology 50 209ndash218 doi101007s002650100363

Payne R (2006) Microbat and small mammal survey ndash Rileys and PelicanIslands Brisbane Water Report prepared for NSW National Parks andWildlife Service Gosford

PennayM Law B and Reinhold L (2004) Bat calls of New SouthWalesregion based guide to the echolocation calls of microchiropteran batsNSW Department of Environment and Conservation Hurstville

Poulin B Lefebvre G and Paz L (2010) Red flag for green spray adversetrophic effects of Bti on breeding birds Journal of Applied Ecology 47884ndash889 doi101111j1365-2664201001821x

Rainho A Augusto A M and Palmeirim J M (2010) Influence ofvegetation clutter on the capacity of ground foraging bats to captureprey Journal of Applied Ecology 47 850ndash858 doi101111j1365-2664201001820x

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Rhodes M P (2002) Assessment of sources of variance and patterns ofoverlap in microchiropteran wing morphology in southeast QueenslandAustralia Canadian Journal of Zoology 80 450ndash460 doi101139z02-029

Rohe D and Fall R (1979) A miniature battery powered CO2 baited lighttrap for mosquito borne encephalitis surveillance Bulletin of the Societyof Vector Ecology 4 24ndash27

Russell R C (1996) lsquoA Colour Photo Atlas of Mosquitoes of SoutheasternAustraliarsquo (TheDepartment ofMedical EntomologyWestmeadHospitaland the University of Sydney Sydney)

Russell T L and Kay B H (2008) Biologically based insecticides forthe control of immature Australian mosquitoes a review AustralianJournal of Entomology 47 232ndash242 doi101111j1440-6055200800642x

Rydell J (1989) Food habits of northem (Eptesicus nilssoni) and brownlong-eared (Plecotus auritus) bats in Sweden Ecography 12 16ndash20doi101111j1600-05871989tb00817x

Saintilan N and Williams R J (1999) Mangrove transgression intosaltmarsh environments in south-east Australia Global Ecology andBiogeography 8 117ndash124 doi101046j1365-2699199900133x

Saunders M B and Barclay R M R (1992) Ecomorphology ofinsectivorous bats a test of predictions using two morphologicallysimilar species Ecology 73 1335ndash1345 doi1023071940680

Scanlon A T and Petit S (2008) Effects of site time weather and light onurban bat activity and richness considerations for survey effortWildlifeResearch 35 821ndash834 doi101071WR08035

Schnitzler H-U and Kalko E K V (2001) Echolocation by insect-eatingbats Bioscience 51 557ndash569 doi1016410006-3568(2001)051[0557EBIEB]20CO2

Speakman J R (1991) The impact of predation by birds on bat populationsin the British Isles Mammal Review 21 123ndash142 doi101111j1365-29071991tb00114x

Specht R L (1970) Vegetation In lsquoThe Australian environmentrsquo 4th edn(Ed F W Leeper) pp 44ndash67 (CSIRO in association with MelbourneUniversity Press Melbourne)

StorkN E andBlackburn TM (1993)Abundance body size and biomassof arthropods in tropical forestOikos 67 483ndash489 doi1023073545360

Do mosquitoes influence bat activity Wildlife Research 23

Taylor L R (1963) Analysis of the effect of temperature on insects in flightJournal of Animal Ecology 32 99ndash117 doi1023072520

Threlfall C Law B Penman T and Banks P B (2011) Ecologicalprocesses in urban landscapes mechanisms influencing the distributionand activity of insectivorous bats Ecography 34 814ndash826 doi101111j1600-0587201006939x

Threlfall C G LawB andBanks P B (2012) Sensitivity of insectivorousbats to urbanization Implications for suburban conservation planningBiological Conservation 146 41ndash52 doi101016jbiocon201111026

Waters D Rydell J and Jones G (1995) Echolocation call design andlimits on prey size a case study using the aerial-hawking bat Nyctalus

leisleri Behavioral Ecology and Sociobiology 37 321ndash328 doi101007BF00174136

Webb C E and Russell R C (2009) Living with mosquitoes in theHunter Region Published by the Department of Medical EntomologyWestmead Hospital and the University of Sydney Sydney

Wickramasinghe L P Harris S Jones G and Vaughan N (2003) Batactivity and species richness on organic and conventional farms impactof agricultural intensification Journal of Applied Ecology 40 984ndash993doi101111j1365-2664200300856x

24 Wildlife Research L Gonsalves et al

wwwpublishcsiroaujournalswr