Hindawi Publishing CorporationInternational Journal of EcologyVolume 2013 Article ID 789532 8 pageshttpdxdoiorg1011552013789532
Research ArticleInfluence of Plant Diversity on the Numerical Response ofEriopis connexa (Coleoptera Coccinellidae) to Changes inCereal Aphid Density in Wheat Crops
Mariacutea C Tulli Dora M Carmona and Ana M Vincini
UI EEA Balcarce INTA-FCA UNMdP Zoologıa Agrıcola Ruta 226 Km 735 Balcarce 7620 Buenos Aires Argentina
Correspondence should be addressed to Marıa C Tulli maricel 46hotmailcom
Received 30 June 2013 Revised 20 October 2013 Accepted 18 November 2013
Academic Editor Jean-Guy Godin
Copyright copy 2013 Marıa C Tulli et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
Cereal aphids cause economic injury to wheat crops In Argentina Eriopis connexa is an indigenous ladybird In the present studythe numerical response of E connexa to changes in aphid density on wheat crops with high and low plant diversity was investigatedThe study was carried out in Balcarce Buenos Aires Argentina from September to December 2007 and 2008 on two wheat cropswith either a higher plant diversity (HPD) with refuge strips or a lower plant diversity (LPD) without refuge strips Crops weresampled every week and the abundance of aphids and E connexa was recorded The dominant aphid species were Schizaphisgraminum Metopolophium dirhodum and Sitobion avenae Eriopis connexa showed a linear increase in the numerical responseto an increase in aphid density which varied in space and time The abundance of E connexa increased in relation to the cropdevelopment and aphid population and was higher in the HPD than in the LPD system This predator increased its reproductivenumerical response only in 2008 with a significant liner response in the HPD systemThis suggests that the potential of E connexaas a predator of cereal aphids also increases directly in proportion to landscape vegetal diversity
1 Introduction
Cereal aphids (Hemiptera Aphididae) are among the mostimportant pests on wheat crops in the world since they arefound in all temperate regions and cropping systems and havethe potential to reduce yields [1 2] Depending on the speciesand the year aphids can cause economic damage by directfeeding by injection of toxins that cause yellowing stuntedgrowth curled leaves andmalformations or by transmissionof viruses that cause indirect plant injury [1ndash4] As a resultaphid damage in wheat crops causes losses in yields and grainquality [5ndash11]
Insecticide application is the strategy selected by farmersto control aphids in wheat crops around the world Howeverthe frequent use of awide range of pesticides has causedmanyside-effects including loss of biodiversity secondary pest out-breaks the development of insect resistance to insecticidesresidual toxicity and suppression of natural enemies [12ndash14]As a consequence promoting the activity of predators andparasitoids in growing systems tomaintain aphid populations
below the economic injury level remains a desirable goal [15]Several groups of natural enemies can control aphid popula-tions in wheat crops such as parasitoid wasps (Hymenopteramainly Aphidiidae) and a very large number of predatorssuch as hoverfly larvae (Diptera Syrphidae) lacewing larvae(Neuroptera Chrysopidae) and ladybird adults and larvae(Coleoptera Coccinellidae) [16 17]
Aphidophagous ladybirds are important predators ofaphids in agricultural crops and have been considered as bio-logical control agents given their ability and voracity to feedon a wide range of prey [18] In Argentina some importantladybird species are Eriopis connexa (Germar) Hippodamiaconvergens (Guerin-Meneville) Coleomegilla quadrifasciata(Schoenherr) Adalia bipunctata (Linnaeus) and Harmoniaaxyridis (Pallas) [19] In Balcarce Buenos Aires provinceArgentina Martinoia [20] determined that the dominantspecies on potato crops is the exotic H axyridis introducedfrom Asia and E connexa an indigenous coccinellid specieswith an exclusive natural distribution in South America [21]Adults of E connexa are 3-4mm length and have a hairless
2 International Journal of Ecology
oval body and the elytra are black with twelve red and whitespots [22 23]
Pest suppression by aphidophagous ladybirds in agri-cultural crops is affected by primary factors such as thecombination of prey and predator densities This results intwo effects each predator increases its consumption ratewhen it is exposed to a higher prey density (functionalresponse) and predator density increases when the prey den-sity also increases (numerical response) However the termldquonumerical responserdquo comprises two different mechanisms ahigher rate of predator reproduction when prey is abundanta ldquoreproductive responserdquo and an attraction of predators toprey aggregations an ldquoaggregational responserdquo [24]
Like many natural enemies adult coccinellids are tran-sient predators foraging within several habitats during thegrowing season [25] For this reason their diversity and abun-dance are expected to depend on both the abundance of preywithin crop habitats and the structure and composition of thesurrounding landscape [24] It has been proven that habitatfeatures such as relative humidity plant density abundanceof alternative foods and other resources provided by plantdiversity of the surrounding crops can influence the spatialdistribution of coccinellids [17 26 27] and other naturalenemies in agricultural landscapes [28ndash34] Characteristicsof the agricultural landscape might influence the numericalresponse of coccinellids However the role of plant diversityin determining the numerical response of native coccinellidsin wheat crops in Argentina has not been investigatedTherefore the main objective of the current study was tocharacterize the numerical response of E connexa to changesin the aphid density on wheat crops with or without theintroduction of a refuge strip to increase plant diversity
2 Materials and Methods
21 Study Site Plant Diversity Management The experimentwas carried out in wheat crops grown with two differentfield management regimes located at the Integrated Unit ofthe Faculty of Agronomy Mar del Plata National Universityand Balcarce Experimental Extension of the National Insti-tute of Agricultural Technology (UIB) (37∘451015840S 58∘181015840W)from August to December 2007 and 2008 The site wasestablished in 2004 and comprised two plots of 6400m2each being 20m apart with different management systemsand representing two environments a crop with a highplant diversity (HPD) with the introduction of refuge stripsand a crop of low plant diversity (LPD) without refugestrips Refuges consisted of 3m-wide strips [30] and 10perennial flowering and aromatic species were planted inthe central half meter Thymus vulgaris Melisa officinalisCoriandrum sativum Artemisia absinthium Lavandula offic-inalis Rosmarinus officinalis Ruta graveolens Salvia offici-nalis Origanum vulgare Calendula officinalis Chrysanthe-mum leucanthemum and Helianthus annuus In additionMedicago sativa was seeded for 1m on each side of therefuge strips [20] These plant species were selected toprovide pollen nectar overwintering refuges and poten-tial prey resources for natural enemies Two small plots
of 1600m2 (40m times 40m) of each environment wereselected for our study and were 60m apart (Figure 1)Each plot was sown with wheat (Klein Chaja) in 175 cmrows at a density of 350 seedsm2 on 10 August 2007 and 6August 2008 During the study there were no applications ofherbicide or insecticide to the crop or refuge strip
22 Sampling Procedure Natural populations of aphids andcoccinellids were sampled weekly from 5 September to 26December 2007 and from 2 September to 22 December 2008Nine sampling sites consisting of four plants were randomlyselected for each sampling date On each sampling date wequantified all the aphids and coccinellids present by carefullyinspecting each plant Larval stages of coccinellids that couldnot be identified were taken to the Service and ResearchUnit of the Agricultural Zoology Laboratory (LISEZA) at theUIB and reared to adulthood in a growth chamber under16L 8D light conditions 22 plusmn 2∘C temperature and 80relative humidity Emerging adults were identified using anOlympus 160x stereoscopic microscope and the taxonomickey of Saini and deColl [22] and the entomological collectionof insects of LIZEZA was used for reference We investigatedthe numerical response of predators by plotting aphid densityagainst concurrent variation in adults and larvae of Econnexa recorded in the same year for each managementsystem
23 Statistical Analysis Our primary analysis applied a gen-eralized estimating equations approach which is appropriatefor longitudinal data because it allows for within subjectrepeated measures examination of change over time as wellas correction of variance estimates for correlated data withinsubject Aphid and coccinellid abundance wasmodeled usinga negative binomial error distribution and a log-link functionspecifying an exchangeable working correlation structurewhich provided a good fit to the data For each environmentthe Wald Statistics using Type III empirical standard erroranalysis was used to test differences between means [35 36]To determine if a relationship existed between the abundanceE connexa and the abundance of aphids a regression modelwas fitted Then an analysis of covariance (ANCOVA) wasperformed to compare between slopes of the regression linesbetween treatments [36] All statistical tests were consideredsignificant at 119875 lt 005
3 Results
31 Species Composition and Seasonal Abundance of Aphidsand Coccinellids on Wheat Crops with a High or Low PlantDiversity The English grain aphid Sitobion avenae (F) therose-grain aphid Metopolophium dirhodum (Walker) andthe greenbug Schizaphis graminum (Rondani) were the mostfrequently recorded aphid species throughout the cereal-growing season Sipha maydis (Passerini) was also identifiedbut its abundancewas very low andwas limited to a few plantssurrounding the plot The English grain aphid was the lastspecies to colonise wheat each season and the most abundantspecies (Table 1 Figure 2)
International Journal of Ecology 3
Refu
ge st
rip
Wheat 2008
2008Wheat
2007
Wheat 2007
HPD
LPD
Refu
ge st
rip
Refu
ge st
rip
80m
180
m
Wheat
Refuge strip
Figure 1 Representative plot to explain the layout of the two treatments of wheat crops with a high plant diversity (HPD) and low plantdiversity (LPD) in 2007-2008 See text for a description of the experimental design
Table 1 Total and relative abundance of aphids on wheat crops with a high (HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Mean values followed by the same letter indicate no significant differences according to the LS means multiple range test at 119875 lt 005
There were significant differences in cereal aphid popu-lations among the two management systems both in 2007and 2008 with most aphids being found in the LPD area(119865118= 88 119875 lt 001) There was no effect of weeks (119865
1518=
1507 NS) and between years aphid abundance was signifi-cantly higher in 2008 than in 2007 (119865
118= 908 119875 lt 001)
The interaction term was nonsignificant (119865118= 377 NS)
The most abundant aphidophagous coccinellid species inwheat crops was E connexa (8576) followed byH axyridis(1068) Coccinella ancoralis (Germ) (148) Scymnusargentinicus (Weise) (104) and Hyperaspis festiva (Mul-sant) (104)
In contrast to aphid populations most E connexa indi-viduals were found in the HPD area (119865
118= 1208 119875 lt 001)
There was no effect of week (1198651518= 135 NS) and between
years the abundance of E connexa was significantly higherin 2008 compared to 2007 (119865
118= 486 119875 lt 005) The inter-
action term was significant (119865118= 535 119875 lt 005)
The aphid population densities in 2007 and 2008increased progressively from October through Novemberand then declined suddenly coincident with the large increasein E connexa and plant physiology changes close to physi-ological maturity (Figure 3) Adults of E connexa increasedin abundance in relation to the development of the crop andaphid abundance which reached its initial highest densityat the end of October after an increase in the abundance ofMetopolophium dirhodum in 2007 and with the increase in Sgraminum and M dirhodum in 2008 Nevertheless in 2008an increase in the abundance ofE connexa in theHPD systemwas observed earlier than in the LPD crop This increase inthe density of E connexa did not result from an increase inthe density of aphids (Figure 3) Eriopis connexa then reachedits second highest density values at the end of Novemberand the beginning of December coincident with the highestabundance of S avenae among the two management systemsin 2007 and 2008
Figure 2 Mean population abundance of Schizaphis graminum Metopolophium dirhodum and Sitobion avenae in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Eriopis connexa showed a linear increase in its aggrega-tional numerical response to aphid density which varied inspace and time In both systems during 2007 and for LPDsystem during 2008 the abundance of E connexa increasedwith an increasing abundance of aphids as indicated bypositive and significant regression coefficients (Figure 4) In2008 the linear regressionmodel was only significant in LPD(Figure 4) Then during 2008 E connexa did not exhibita numerical response to change in aphis density in HPD(Figure 4)
During 2007 (ANCOVA t-test = 045 NS) and 2008(ANCOVA t-test = 017 NS) there were no significantchanges in the aggregational numerical response betweenmanagement systems However in 2008 we registered anincrease in the reproductive numerical response which wasgreater for the HPD system (ANCOVA t-test = 295 119875 lt005) (Figure 5)The presence of the first immature individu-als was recorded at the end of October and at the beginningof September and in both systems the peak population of
E connexa larvae was recorded in mid-November Similar toadults of E connexa most immature individuals were foundin the HPD area (119865
17= 466 119875 lt 005) and there was
no effect of weeks (11986567= 58 NS) During this period the
number of larvae increased but no superposition of differentlarval stages within these stages was registered
4 Discussion
Our analysis of the population density of E connexa andcereal aphids showed that trophic interactions in wheat fieldsvaried greatly between years and depended on plant diversitysurrounding the wheat cropThe results showed that increas-ing the structural complexity of the habitat surroundingwheat crops resulted in a higher abundance of E connexathat would account for the smaller abundance of cerealaphids registered in the HPD systems Similar conclusionswere reached in previous studies where the increase in plantdiversity in wheat crops increased the number of larvae of
International Journal of Ecology 5
HPD 2007
0
2
4
6
8
10
12
14M
ean
num
ber o
f aph
ids
tille
r
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(a)
LPD 2007
0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(b)
HPD 2008
Aphids Eriopis connexa adults
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(c)
LPD 2008
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
Aphids Eriopis connexa adults
(d)
Figure 3 Seasonal abundance of aphid and adults of Eriopis connexa in wheat crops with a high (HPD) and low plant diversity (LPD)Balcarce 2007 and 2008 Mean number of aphids per tiller plusmn SE and mean number of Eriopis connexa per tiller plusmn SE
hoverflies and coccinellids [26] and aphid parasitism [34 37]Studies in other crops likewise concluded that protectingthe natural vegetation surrounding agroecosystems [27 38]andor introducing plant species into strips as a refuge arepractices that increase natural enemy abundance in cultivatedareas prone to pests [13 20 30 31]
In the current study the regression models indicated thatadults and larvae of E connexawere more abundant in wheatfields when aphids were abundant than when they were notUnsurprisingly the numerical responses of E connexa wereaffected by cereal aphid abundance but the most importantresults of this study support the view that E connexa dynam-ics is not only exclusively related to prey abundance but alsoto plant diversity The positive effect of plant diversity onthe reproductive numerical response is a consequence of thedependence of emerged ladybeetles in early spring on preyin hibernation areas when aphid densities in the fields arestill low Since the level of food supply affects the fecundity
[39ndash41] and migration behavior of ladybeetles [39] theavailability of aphids in noncrop landscape elements is likelyto impact the numbers and distribution of ladybeetles andassociated biocontrol in agro-ecosystems [13]Moreover preyavailability in shelter habitats in early spring can influencepostoverwintering mortality the fecundity of surviving coc-cinellids and the phenology of dispersal into the crop [42]In this study we registered this type of effect because during2008 we recorded an increase in the abundance of E connexaearlier in the HPD crop than in the LPD crop This increasein the density of E connexa did not result from an increase inthe density of cereal aphids Even if the abundance of cerealaphids could not account for that of E connexa within thisperiod the presence of this coccinellid in the crops could beexplained as a direct effect of the refuge strip During theautumn of 2008 an increase in the abundance of aphids onM sativawas observedThe presence of aphids in the refugesfavored predator survival and increased their abundance
6 International Journal of Ecology
HPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
y = 025x minus 016
R2 =
(F115 = 3107 P lt 005)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
069
(a)
LPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
y = 021x + 005
028558 P lt 005)
(b)
HPD 2008
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
(F115 = 242NS)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
y = 008x + 046
015
(c)
LPD 2008
0 2 4 6 8 100
03
06
09
12
15
18
y =
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
008x + 002
035558 P lt 005)
(d)
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
oval body and the elytra are black with twelve red and whitespots [22 23]
Pest suppression by aphidophagous ladybirds in agri-cultural crops is affected by primary factors such as thecombination of prey and predator densities This results intwo effects each predator increases its consumption ratewhen it is exposed to a higher prey density (functionalresponse) and predator density increases when the prey den-sity also increases (numerical response) However the termldquonumerical responserdquo comprises two different mechanisms ahigher rate of predator reproduction when prey is abundanta ldquoreproductive responserdquo and an attraction of predators toprey aggregations an ldquoaggregational responserdquo [24]
Like many natural enemies adult coccinellids are tran-sient predators foraging within several habitats during thegrowing season [25] For this reason their diversity and abun-dance are expected to depend on both the abundance of preywithin crop habitats and the structure and composition of thesurrounding landscape [24] It has been proven that habitatfeatures such as relative humidity plant density abundanceof alternative foods and other resources provided by plantdiversity of the surrounding crops can influence the spatialdistribution of coccinellids [17 26 27] and other naturalenemies in agricultural landscapes [28ndash34] Characteristicsof the agricultural landscape might influence the numericalresponse of coccinellids However the role of plant diversityin determining the numerical response of native coccinellidsin wheat crops in Argentina has not been investigatedTherefore the main objective of the current study was tocharacterize the numerical response of E connexa to changesin the aphid density on wheat crops with or without theintroduction of a refuge strip to increase plant diversity
2 Materials and Methods
21 Study Site Plant Diversity Management The experimentwas carried out in wheat crops grown with two differentfield management regimes located at the Integrated Unit ofthe Faculty of Agronomy Mar del Plata National Universityand Balcarce Experimental Extension of the National Insti-tute of Agricultural Technology (UIB) (37∘451015840S 58∘181015840W)from August to December 2007 and 2008 The site wasestablished in 2004 and comprised two plots of 6400m2each being 20m apart with different management systemsand representing two environments a crop with a highplant diversity (HPD) with the introduction of refuge stripsand a crop of low plant diversity (LPD) without refugestrips Refuges consisted of 3m-wide strips [30] and 10perennial flowering and aromatic species were planted inthe central half meter Thymus vulgaris Melisa officinalisCoriandrum sativum Artemisia absinthium Lavandula offic-inalis Rosmarinus officinalis Ruta graveolens Salvia offici-nalis Origanum vulgare Calendula officinalis Chrysanthe-mum leucanthemum and Helianthus annuus In additionMedicago sativa was seeded for 1m on each side of therefuge strips [20] These plant species were selected toprovide pollen nectar overwintering refuges and poten-tial prey resources for natural enemies Two small plots
of 1600m2 (40m times 40m) of each environment wereselected for our study and were 60m apart (Figure 1)Each plot was sown with wheat (Klein Chaja) in 175 cmrows at a density of 350 seedsm2 on 10 August 2007 and 6August 2008 During the study there were no applications ofherbicide or insecticide to the crop or refuge strip
22 Sampling Procedure Natural populations of aphids andcoccinellids were sampled weekly from 5 September to 26December 2007 and from 2 September to 22 December 2008Nine sampling sites consisting of four plants were randomlyselected for each sampling date On each sampling date wequantified all the aphids and coccinellids present by carefullyinspecting each plant Larval stages of coccinellids that couldnot be identified were taken to the Service and ResearchUnit of the Agricultural Zoology Laboratory (LISEZA) at theUIB and reared to adulthood in a growth chamber under16L 8D light conditions 22 plusmn 2∘C temperature and 80relative humidity Emerging adults were identified using anOlympus 160x stereoscopic microscope and the taxonomickey of Saini and deColl [22] and the entomological collectionof insects of LIZEZA was used for reference We investigatedthe numerical response of predators by plotting aphid densityagainst concurrent variation in adults and larvae of Econnexa recorded in the same year for each managementsystem
23 Statistical Analysis Our primary analysis applied a gen-eralized estimating equations approach which is appropriatefor longitudinal data because it allows for within subjectrepeated measures examination of change over time as wellas correction of variance estimates for correlated data withinsubject Aphid and coccinellid abundance wasmodeled usinga negative binomial error distribution and a log-link functionspecifying an exchangeable working correlation structurewhich provided a good fit to the data For each environmentthe Wald Statistics using Type III empirical standard erroranalysis was used to test differences between means [35 36]To determine if a relationship existed between the abundanceE connexa and the abundance of aphids a regression modelwas fitted Then an analysis of covariance (ANCOVA) wasperformed to compare between slopes of the regression linesbetween treatments [36] All statistical tests were consideredsignificant at 119875 lt 005
3 Results
31 Species Composition and Seasonal Abundance of Aphidsand Coccinellids on Wheat Crops with a High or Low PlantDiversity The English grain aphid Sitobion avenae (F) therose-grain aphid Metopolophium dirhodum (Walker) andthe greenbug Schizaphis graminum (Rondani) were the mostfrequently recorded aphid species throughout the cereal-growing season Sipha maydis (Passerini) was also identifiedbut its abundancewas very low andwas limited to a few plantssurrounding the plot The English grain aphid was the lastspecies to colonise wheat each season and the most abundantspecies (Table 1 Figure 2)
International Journal of Ecology 3
Refu
ge st
rip
Wheat 2008
2008Wheat
2007
Wheat 2007
HPD
LPD
Refu
ge st
rip
Refu
ge st
rip
80m
180
m
Wheat
Refuge strip
Figure 1 Representative plot to explain the layout of the two treatments of wheat crops with a high plant diversity (HPD) and low plantdiversity (LPD) in 2007-2008 See text for a description of the experimental design
Table 1 Total and relative abundance of aphids on wheat crops with a high (HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Mean values followed by the same letter indicate no significant differences according to the LS means multiple range test at 119875 lt 005
There were significant differences in cereal aphid popu-lations among the two management systems both in 2007and 2008 with most aphids being found in the LPD area(119865118= 88 119875 lt 001) There was no effect of weeks (119865
1518=
1507 NS) and between years aphid abundance was signifi-cantly higher in 2008 than in 2007 (119865
118= 908 119875 lt 001)
The interaction term was nonsignificant (119865118= 377 NS)
The most abundant aphidophagous coccinellid species inwheat crops was E connexa (8576) followed byH axyridis(1068) Coccinella ancoralis (Germ) (148) Scymnusargentinicus (Weise) (104) and Hyperaspis festiva (Mul-sant) (104)
In contrast to aphid populations most E connexa indi-viduals were found in the HPD area (119865
118= 1208 119875 lt 001)
There was no effect of week (1198651518= 135 NS) and between
years the abundance of E connexa was significantly higherin 2008 compared to 2007 (119865
118= 486 119875 lt 005) The inter-
action term was significant (119865118= 535 119875 lt 005)
The aphid population densities in 2007 and 2008increased progressively from October through Novemberand then declined suddenly coincident with the large increasein E connexa and plant physiology changes close to physi-ological maturity (Figure 3) Adults of E connexa increasedin abundance in relation to the development of the crop andaphid abundance which reached its initial highest densityat the end of October after an increase in the abundance ofMetopolophium dirhodum in 2007 and with the increase in Sgraminum and M dirhodum in 2008 Nevertheless in 2008an increase in the abundance ofE connexa in theHPD systemwas observed earlier than in the LPD crop This increase inthe density of E connexa did not result from an increase inthe density of aphids (Figure 3) Eriopis connexa then reachedits second highest density values at the end of Novemberand the beginning of December coincident with the highestabundance of S avenae among the two management systemsin 2007 and 2008
Figure 2 Mean population abundance of Schizaphis graminum Metopolophium dirhodum and Sitobion avenae in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Eriopis connexa showed a linear increase in its aggrega-tional numerical response to aphid density which varied inspace and time In both systems during 2007 and for LPDsystem during 2008 the abundance of E connexa increasedwith an increasing abundance of aphids as indicated bypositive and significant regression coefficients (Figure 4) In2008 the linear regressionmodel was only significant in LPD(Figure 4) Then during 2008 E connexa did not exhibita numerical response to change in aphis density in HPD(Figure 4)
During 2007 (ANCOVA t-test = 045 NS) and 2008(ANCOVA t-test = 017 NS) there were no significantchanges in the aggregational numerical response betweenmanagement systems However in 2008 we registered anincrease in the reproductive numerical response which wasgreater for the HPD system (ANCOVA t-test = 295 119875 lt005) (Figure 5)The presence of the first immature individu-als was recorded at the end of October and at the beginningof September and in both systems the peak population of
E connexa larvae was recorded in mid-November Similar toadults of E connexa most immature individuals were foundin the HPD area (119865
17= 466 119875 lt 005) and there was
no effect of weeks (11986567= 58 NS) During this period the
number of larvae increased but no superposition of differentlarval stages within these stages was registered
4 Discussion
Our analysis of the population density of E connexa andcereal aphids showed that trophic interactions in wheat fieldsvaried greatly between years and depended on plant diversitysurrounding the wheat cropThe results showed that increas-ing the structural complexity of the habitat surroundingwheat crops resulted in a higher abundance of E connexathat would account for the smaller abundance of cerealaphids registered in the HPD systems Similar conclusionswere reached in previous studies where the increase in plantdiversity in wheat crops increased the number of larvae of
International Journal of Ecology 5
HPD 2007
0
2
4
6
8
10
12
14M
ean
num
ber o
f aph
ids
tille
r
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(a)
LPD 2007
0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(b)
HPD 2008
Aphids Eriopis connexa adults
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(c)
LPD 2008
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
Aphids Eriopis connexa adults
(d)
Figure 3 Seasonal abundance of aphid and adults of Eriopis connexa in wheat crops with a high (HPD) and low plant diversity (LPD)Balcarce 2007 and 2008 Mean number of aphids per tiller plusmn SE and mean number of Eriopis connexa per tiller plusmn SE
hoverflies and coccinellids [26] and aphid parasitism [34 37]Studies in other crops likewise concluded that protectingthe natural vegetation surrounding agroecosystems [27 38]andor introducing plant species into strips as a refuge arepractices that increase natural enemy abundance in cultivatedareas prone to pests [13 20 30 31]
In the current study the regression models indicated thatadults and larvae of E connexawere more abundant in wheatfields when aphids were abundant than when they were notUnsurprisingly the numerical responses of E connexa wereaffected by cereal aphid abundance but the most importantresults of this study support the view that E connexa dynam-ics is not only exclusively related to prey abundance but alsoto plant diversity The positive effect of plant diversity onthe reproductive numerical response is a consequence of thedependence of emerged ladybeetles in early spring on preyin hibernation areas when aphid densities in the fields arestill low Since the level of food supply affects the fecundity
[39ndash41] and migration behavior of ladybeetles [39] theavailability of aphids in noncrop landscape elements is likelyto impact the numbers and distribution of ladybeetles andassociated biocontrol in agro-ecosystems [13]Moreover preyavailability in shelter habitats in early spring can influencepostoverwintering mortality the fecundity of surviving coc-cinellids and the phenology of dispersal into the crop [42]In this study we registered this type of effect because during2008 we recorded an increase in the abundance of E connexaearlier in the HPD crop than in the LPD crop This increasein the density of E connexa did not result from an increase inthe density of cereal aphids Even if the abundance of cerealaphids could not account for that of E connexa within thisperiod the presence of this coccinellid in the crops could beexplained as a direct effect of the refuge strip During theautumn of 2008 an increase in the abundance of aphids onM sativawas observedThe presence of aphids in the refugesfavored predator survival and increased their abundance
6 International Journal of Ecology
HPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
y = 025x minus 016
R2 =
(F115 = 3107 P lt 005)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
069
(a)
LPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
y = 021x + 005
028558 P lt 005)
(b)
HPD 2008
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
(F115 = 242NS)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
y = 008x + 046
015
(c)
LPD 2008
0 2 4 6 8 100
03
06
09
12
15
18
y =
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
008x + 002
035558 P lt 005)
(d)
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
Figure 1 Representative plot to explain the layout of the two treatments of wheat crops with a high plant diversity (HPD) and low plantdiversity (LPD) in 2007-2008 See text for a description of the experimental design
Table 1 Total and relative abundance of aphids on wheat crops with a high (HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Mean values followed by the same letter indicate no significant differences according to the LS means multiple range test at 119875 lt 005
There were significant differences in cereal aphid popu-lations among the two management systems both in 2007and 2008 with most aphids being found in the LPD area(119865118= 88 119875 lt 001) There was no effect of weeks (119865
1518=
1507 NS) and between years aphid abundance was signifi-cantly higher in 2008 than in 2007 (119865
118= 908 119875 lt 001)
The interaction term was nonsignificant (119865118= 377 NS)
The most abundant aphidophagous coccinellid species inwheat crops was E connexa (8576) followed byH axyridis(1068) Coccinella ancoralis (Germ) (148) Scymnusargentinicus (Weise) (104) and Hyperaspis festiva (Mul-sant) (104)
In contrast to aphid populations most E connexa indi-viduals were found in the HPD area (119865
118= 1208 119875 lt 001)
There was no effect of week (1198651518= 135 NS) and between
years the abundance of E connexa was significantly higherin 2008 compared to 2007 (119865
118= 486 119875 lt 005) The inter-
action term was significant (119865118= 535 119875 lt 005)
The aphid population densities in 2007 and 2008increased progressively from October through Novemberand then declined suddenly coincident with the large increasein E connexa and plant physiology changes close to physi-ological maturity (Figure 3) Adults of E connexa increasedin abundance in relation to the development of the crop andaphid abundance which reached its initial highest densityat the end of October after an increase in the abundance ofMetopolophium dirhodum in 2007 and with the increase in Sgraminum and M dirhodum in 2008 Nevertheless in 2008an increase in the abundance ofE connexa in theHPD systemwas observed earlier than in the LPD crop This increase inthe density of E connexa did not result from an increase inthe density of aphids (Figure 3) Eriopis connexa then reachedits second highest density values at the end of Novemberand the beginning of December coincident with the highestabundance of S avenae among the two management systemsin 2007 and 2008
Figure 2 Mean population abundance of Schizaphis graminum Metopolophium dirhodum and Sitobion avenae in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Eriopis connexa showed a linear increase in its aggrega-tional numerical response to aphid density which varied inspace and time In both systems during 2007 and for LPDsystem during 2008 the abundance of E connexa increasedwith an increasing abundance of aphids as indicated bypositive and significant regression coefficients (Figure 4) In2008 the linear regressionmodel was only significant in LPD(Figure 4) Then during 2008 E connexa did not exhibita numerical response to change in aphis density in HPD(Figure 4)
During 2007 (ANCOVA t-test = 045 NS) and 2008(ANCOVA t-test = 017 NS) there were no significantchanges in the aggregational numerical response betweenmanagement systems However in 2008 we registered anincrease in the reproductive numerical response which wasgreater for the HPD system (ANCOVA t-test = 295 119875 lt005) (Figure 5)The presence of the first immature individu-als was recorded at the end of October and at the beginningof September and in both systems the peak population of
E connexa larvae was recorded in mid-November Similar toadults of E connexa most immature individuals were foundin the HPD area (119865
17= 466 119875 lt 005) and there was
no effect of weeks (11986567= 58 NS) During this period the
number of larvae increased but no superposition of differentlarval stages within these stages was registered
4 Discussion
Our analysis of the population density of E connexa andcereal aphids showed that trophic interactions in wheat fieldsvaried greatly between years and depended on plant diversitysurrounding the wheat cropThe results showed that increas-ing the structural complexity of the habitat surroundingwheat crops resulted in a higher abundance of E connexathat would account for the smaller abundance of cerealaphids registered in the HPD systems Similar conclusionswere reached in previous studies where the increase in plantdiversity in wheat crops increased the number of larvae of
International Journal of Ecology 5
HPD 2007
0
2
4
6
8
10
12
14M
ean
num
ber o
f aph
ids
tille
r
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(a)
LPD 2007
0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(b)
HPD 2008
Aphids Eriopis connexa adults
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(c)
LPD 2008
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
Aphids Eriopis connexa adults
(d)
Figure 3 Seasonal abundance of aphid and adults of Eriopis connexa in wheat crops with a high (HPD) and low plant diversity (LPD)Balcarce 2007 and 2008 Mean number of aphids per tiller plusmn SE and mean number of Eriopis connexa per tiller plusmn SE
hoverflies and coccinellids [26] and aphid parasitism [34 37]Studies in other crops likewise concluded that protectingthe natural vegetation surrounding agroecosystems [27 38]andor introducing plant species into strips as a refuge arepractices that increase natural enemy abundance in cultivatedareas prone to pests [13 20 30 31]
In the current study the regression models indicated thatadults and larvae of E connexawere more abundant in wheatfields when aphids were abundant than when they were notUnsurprisingly the numerical responses of E connexa wereaffected by cereal aphid abundance but the most importantresults of this study support the view that E connexa dynam-ics is not only exclusively related to prey abundance but alsoto plant diversity The positive effect of plant diversity onthe reproductive numerical response is a consequence of thedependence of emerged ladybeetles in early spring on preyin hibernation areas when aphid densities in the fields arestill low Since the level of food supply affects the fecundity
[39ndash41] and migration behavior of ladybeetles [39] theavailability of aphids in noncrop landscape elements is likelyto impact the numbers and distribution of ladybeetles andassociated biocontrol in agro-ecosystems [13]Moreover preyavailability in shelter habitats in early spring can influencepostoverwintering mortality the fecundity of surviving coc-cinellids and the phenology of dispersal into the crop [42]In this study we registered this type of effect because during2008 we recorded an increase in the abundance of E connexaearlier in the HPD crop than in the LPD crop This increasein the density of E connexa did not result from an increase inthe density of cereal aphids Even if the abundance of cerealaphids could not account for that of E connexa within thisperiod the presence of this coccinellid in the crops could beexplained as a direct effect of the refuge strip During theautumn of 2008 an increase in the abundance of aphids onM sativawas observedThe presence of aphids in the refugesfavored predator survival and increased their abundance
6 International Journal of Ecology
HPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
y = 025x minus 016
R2 =
(F115 = 3107 P lt 005)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
069
(a)
LPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
y = 021x + 005
028558 P lt 005)
(b)
HPD 2008
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
(F115 = 242NS)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
y = 008x + 046
015
(c)
LPD 2008
0 2 4 6 8 100
03
06
09
12
15
18
y =
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
008x + 002
035558 P lt 005)
(d)
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
Figure 2 Mean population abundance of Schizaphis graminum Metopolophium dirhodum and Sitobion avenae in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2007 and 2008
Eriopis connexa showed a linear increase in its aggrega-tional numerical response to aphid density which varied inspace and time In both systems during 2007 and for LPDsystem during 2008 the abundance of E connexa increasedwith an increasing abundance of aphids as indicated bypositive and significant regression coefficients (Figure 4) In2008 the linear regressionmodel was only significant in LPD(Figure 4) Then during 2008 E connexa did not exhibita numerical response to change in aphis density in HPD(Figure 4)
During 2007 (ANCOVA t-test = 045 NS) and 2008(ANCOVA t-test = 017 NS) there were no significantchanges in the aggregational numerical response betweenmanagement systems However in 2008 we registered anincrease in the reproductive numerical response which wasgreater for the HPD system (ANCOVA t-test = 295 119875 lt005) (Figure 5)The presence of the first immature individu-als was recorded at the end of October and at the beginningof September and in both systems the peak population of
E connexa larvae was recorded in mid-November Similar toadults of E connexa most immature individuals were foundin the HPD area (119865
17= 466 119875 lt 005) and there was
no effect of weeks (11986567= 58 NS) During this period the
number of larvae increased but no superposition of differentlarval stages within these stages was registered
4 Discussion
Our analysis of the population density of E connexa andcereal aphids showed that trophic interactions in wheat fieldsvaried greatly between years and depended on plant diversitysurrounding the wheat cropThe results showed that increas-ing the structural complexity of the habitat surroundingwheat crops resulted in a higher abundance of E connexathat would account for the smaller abundance of cerealaphids registered in the HPD systems Similar conclusionswere reached in previous studies where the increase in plantdiversity in wheat crops increased the number of larvae of
International Journal of Ecology 5
HPD 2007
0
2
4
6
8
10
12
14M
ean
num
ber o
f aph
ids
tille
r
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(a)
LPD 2007
0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
September October November December
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(b)
HPD 2008
Aphids Eriopis connexa adults
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
(c)
LPD 2008
September October November December0
2
4
6
8
10
12
14
Mea
n nu
mbe
r of a
phid
stil
ler
Mea
n nu
mbe
r of E
riopi
s con
nexa
tille
r
0
04
08
12
16
2
Aphids Eriopis connexa adults
(d)
Figure 3 Seasonal abundance of aphid and adults of Eriopis connexa in wheat crops with a high (HPD) and low plant diversity (LPD)Balcarce 2007 and 2008 Mean number of aphids per tiller plusmn SE and mean number of Eriopis connexa per tiller plusmn SE
hoverflies and coccinellids [26] and aphid parasitism [34 37]Studies in other crops likewise concluded that protectingthe natural vegetation surrounding agroecosystems [27 38]andor introducing plant species into strips as a refuge arepractices that increase natural enemy abundance in cultivatedareas prone to pests [13 20 30 31]
In the current study the regression models indicated thatadults and larvae of E connexawere more abundant in wheatfields when aphids were abundant than when they were notUnsurprisingly the numerical responses of E connexa wereaffected by cereal aphid abundance but the most importantresults of this study support the view that E connexa dynam-ics is not only exclusively related to prey abundance but alsoto plant diversity The positive effect of plant diversity onthe reproductive numerical response is a consequence of thedependence of emerged ladybeetles in early spring on preyin hibernation areas when aphid densities in the fields arestill low Since the level of food supply affects the fecundity
[39ndash41] and migration behavior of ladybeetles [39] theavailability of aphids in noncrop landscape elements is likelyto impact the numbers and distribution of ladybeetles andassociated biocontrol in agro-ecosystems [13]Moreover preyavailability in shelter habitats in early spring can influencepostoverwintering mortality the fecundity of surviving coc-cinellids and the phenology of dispersal into the crop [42]In this study we registered this type of effect because during2008 we recorded an increase in the abundance of E connexaearlier in the HPD crop than in the LPD crop This increasein the density of E connexa did not result from an increase inthe density of cereal aphids Even if the abundance of cerealaphids could not account for that of E connexa within thisperiod the presence of this coccinellid in the crops could beexplained as a direct effect of the refuge strip During theautumn of 2008 an increase in the abundance of aphids onM sativawas observedThe presence of aphids in the refugesfavored predator survival and increased their abundance
6 International Journal of Ecology
HPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
y = 025x minus 016
R2 =
(F115 = 3107 P lt 005)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
069
(a)
LPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
y = 021x + 005
028558 P lt 005)
(b)
HPD 2008
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
(F115 = 242NS)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
y = 008x + 046
015
(c)
LPD 2008
0 2 4 6 8 100
03
06
09
12
15
18
y =
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
008x + 002
035558 P lt 005)
(d)
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
Figure 3 Seasonal abundance of aphid and adults of Eriopis connexa in wheat crops with a high (HPD) and low plant diversity (LPD)Balcarce 2007 and 2008 Mean number of aphids per tiller plusmn SE and mean number of Eriopis connexa per tiller plusmn SE
hoverflies and coccinellids [26] and aphid parasitism [34 37]Studies in other crops likewise concluded that protectingthe natural vegetation surrounding agroecosystems [27 38]andor introducing plant species into strips as a refuge arepractices that increase natural enemy abundance in cultivatedareas prone to pests [13 20 30 31]
In the current study the regression models indicated thatadults and larvae of E connexawere more abundant in wheatfields when aphids were abundant than when they were notUnsurprisingly the numerical responses of E connexa wereaffected by cereal aphid abundance but the most importantresults of this study support the view that E connexa dynam-ics is not only exclusively related to prey abundance but alsoto plant diversity The positive effect of plant diversity onthe reproductive numerical response is a consequence of thedependence of emerged ladybeetles in early spring on preyin hibernation areas when aphid densities in the fields arestill low Since the level of food supply affects the fecundity
[39ndash41] and migration behavior of ladybeetles [39] theavailability of aphids in noncrop landscape elements is likelyto impact the numbers and distribution of ladybeetles andassociated biocontrol in agro-ecosystems [13]Moreover preyavailability in shelter habitats in early spring can influencepostoverwintering mortality the fecundity of surviving coc-cinellids and the phenology of dispersal into the crop [42]In this study we registered this type of effect because during2008 we recorded an increase in the abundance of E connexaearlier in the HPD crop than in the LPD crop This increasein the density of E connexa did not result from an increase inthe density of cereal aphids Even if the abundance of cerealaphids could not account for that of E connexa within thisperiod the presence of this coccinellid in the crops could beexplained as a direct effect of the refuge strip During theautumn of 2008 an increase in the abundance of aphids onM sativawas observedThe presence of aphids in the refugesfavored predator survival and increased their abundance
6 International Journal of Ecology
HPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
y = 025x minus 016
R2 =
(F115 = 3107 P lt 005)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
069
(a)
LPD 2007
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
y = 021x + 005
028558 P lt 005)
(b)
HPD 2008
0
03
06
09
12
15
18
0 2 4 6 8 10
R2 =
(F115 = 242NS)
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
y = 008x + 046
015
(c)
LPD 2008
0 2 4 6 8 100
03
06
09
12
15
18
y =
R2 =
Mean number of aphidstiller
Mea
n nu
mbe
r of E
riopi
s con
nexa
adul
ttill
er
(F115 =
008x + 002
035558 P lt 005)
(d)
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
Figure 4 Aggregative numerical response of Eriopis connexa adults to variation in cereal aphid abundance in wheat crops with a high (HPD)and low plant diversity (LPD) Balcarce 2007 and 2008
Mean number of aphidstiller
HPD 2008
0 2 4 6 8 100
04
08
12
16
2
24
R2 =
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 032x minus 052
059
2007 P lt 005)
(a)
LPD 2008
0
04
08
12
16
2
24
0 2 4 6 8 10
R2 =
Mean number of aphidstiller
(F115 =
Mea
n nu
mbe
r of E
riopi
s con
nexa
larv
aeti
ller
y = 0076x minus 0005
017
558 P lt 005)
(b)
Figure 5 Reproductive numerical response of Eriopis connexa larvae to variation in cereal aphid abundance in wheat crops with a high(HPD) and low plant diversity (LPD) Balcarce 2008
International Journal of Ecology 7
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
before the early stage of wheat sowing Furthermore the pres-ence of aphids in the refuges could be explained by the betterreproductive performance of adult E connexa and conse-quently the presence of larvae during 2008 Egg productionin aphidophaga is usually related solely to the availability ofprey However some studies have indicated that fecundityis also influenced by the prey quality [43] Our results areconsistent with those of Bianchi and van der Werf [44] whoestablished that reproduction and the associated control ofpest aphids are affected by both the availability of nonpestaphids in noncrop habitats and the infestation date of pestaphids in wheat fields When the infestation of wheat by pestaphids occurs early in the season the prey availability of pestaphids alone is sufficient to allow C septempunctata to attainitsmaximumreproductionHowever when the infestation bypest aphids is somewhat delayed C septempunctata becomesincreasingly dependent on aphids in noncrop habitatsThere-fore prey availability in noncrop habitats might play asignificant role in the conservation of ladybeetles and directlyaffect the numerical response of predators and consequentlythe biological control of cereal aphids in agroecosystems
It might be possible to enhance the population of coc-cinellids in the agricultural landscape by increasing plantdiversity Plant diversity supports prey diversity and providesrefuge and additional resources such as pollen and nectarfecundity [13 31ndash33] As a result coccinellids and othernatural enemies should be able to respond better to thechange in aphid densities in diverse habitats In agriculturallandscapes it might be possible to enhance populations ofcoccinellids by manipulating plant diversity The presence ofrefuges near wheat crops is particularly important in deter-mining the local abundance of E connexa The augmentationof prey availability in noncrop habitats is one of the habitatmanagement strategies that might preserve predators inagricultural landscapes and increase their effectiveness [13]Moreover individual predators might not need to travel farto obtain essential resources This suggests that the potentialof E connexa as a predator of cereal aphids also increasesdirectly in proportion to landscape vegetal diversity
5 Conclusions
In summary we observed an increase in the numericalresponse of E connexa in an HPD system as measured by anincrease in their abundance reproduction and early seasonalactivity For E connexa we demonstrated that enhancingplant diversity can result in an increase in the populationabundance of this coccinellid predator Even though anincrease in plant diversity in the agroecosystems and itsmain-tenance represents an additional cost for farmers predatorefficacy would increase over time and consequently pestattack would be less likely to cause economically importantdamage
Acknowledgments
Theauthors are grateful to the editor Jean-GuyGodin and oneanonymous reviewer for the valuable comments on earlierdrafts of this paper
References
[1] V O Sadras A Fereres and R H Ratcliffe ldquoWheat growthyield and quality as affected by insect herbivoresrdquo in WheatEcology and Physiology of Yield Determination E H Satorreand G A Slafer Eds pp 183ndash211 Food Products Press TheHaworth Press Binghamton NY USA 1999
[2] H F van Emden and R Harrington Eds Aphids as Crop PestsCABI Wallingford UK 2007
[3] R H Quintanilla Pulgones Caracterısticas morfologicas ybiologicas Especies de mayor importancia agrıcola HemisferioSur Buenos Aires Argentina 1976
[4] A M Vincini A N Lopez and D Sisti Presencia del ldquopulgonde la avenardquo Rophalosiphum padi en el sudeste bonaerense IPEProd Veg INTA Balcarce Argentina 1982
[5] R L Carrillo M Z Mellazo and A B Pino ldquoLos afidos Sito-bium avenae (Fabricius) y Metopolophium dirhodum (Walk)Su influencia en el rendimiento ubicacion en la planta y susenemigos naturalesrdquo Agro Sur vol 2 no 2 pp 71ndash85 1974
[6] C Torres C Senigagliesi R Parisi and AMottioli ldquoIncidenciadel pulgon amarillo de los cereales Metopolophium dirhodumWalk en el cultivo de Trigordquo Informe Tecnico 134 INTAEstacion experimental 1976
[7] G Lee D J Stevens S Stokes and S D Wratten ldquoDurationof cereal aphid populations and the effects on wheat yield andbreadmaking qualityrdquo Annals of Applied Biology vol 98 no 2pp 169ndash178 1981
[8] P R Holmes ldquoA field study of the predators of the grain aphidSitobion avenae (F) ( Hemiptera Aphididae) in winter wheatin Britainrdquo Bulletin of Entomological Research vol 74 no 4 pp623ndash631 1984
[9] R W Kieckhefer and B H Kantack ldquoYield losses in wintergrains caused by cereal aphids (Homoptera Aphididae) inSouthDakotardquo Journal of Economic Entomology vol 81 pp 317ndash321 1988
[10] R W Kieckhefer and J L Gellner ldquoYield losses in winter wheatcaused by low-density cereal aphid populationsrdquo AgronomyJournal vol 84 no 2 pp 180ndash183 1992
[11] J N Oakley and K F A Walters ldquoA field evaluation of differentcriteria for determining the need to treat winter wheat againstthe grain aphid Sitobion avenae and the rose-grain aphidMetopolophium dirhodumrdquo Annals of Applied Biology vol 124no 2 pp 195ndash211 1994
[12] R G van Driesche and T S Bellows Biological ControlChapman amp Hall New York NY USA 1996
[13] D Landis F D Menalled J Lee D M Carmona and A PValdez ldquoHabitat management to enhance biological control inIPMrdquo in Emerging Technologies for Integrated Pest ManagementConcepts Research and Implementation G G Kenedy and T BSutton Eds pp 226ndash239 APS Press St PaulMinn USA 2000
[14] A E Hajek ldquoWhy use natural enemiesrdquo in Natural EnemiesAn Introduction to Biological Control pp 3ndash18 CambridgeUniversity Press Cambridge UK 2004
[15] A K Fiedler D A Landis and S DWratten ldquoMaximizing eco-system services from conservation biological control the role ofhabitat managementrdquo Biological Control vol 45 no 2 pp 254ndash271 2008
[16] C Salto J Lopez I Bertolaccini and J Imwinkelried ldquoObser-vaciones preliminares de las interacciones malezas-fitofagos-enemigos naturales en el area central de la Provincia de SantaFerdquo Gaceta Agronomica vol 12 no 71 pp 21ndash30 1993
8 International Journal of Ecology
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
[17] M J Brewer and N C Elliott ldquoBiological control of cerealaphids in North America andmediating efects of host plant andhabitat manipulationsrdquo Annual Review of Entomology vol 49pp 219ndash242 2004
[18] J J Obrycki and T J Kring ldquoPredaceous coccinellidae inbiological controlrdquo Annual Review of Entomology vol 43 pp295ndash321 1998
[19] E D Saini ldquoPresencia de Harmonia axyridis (Pallas) (Cole-optera Coccinellidae) en la provincia de Buenos Airesrdquo Aspec-tos Biologicos y Morfologicos RIA vol 33 no 1 pp 151ndash1602004
[20] G Martinoia Fluctuacion poblacional de pulgones (HemipteraAphididae) y sus reguladores naturales (Coleoptera Coccinelli-dae) en cultivos de papa con refugios vegetales y uso oportunode plaguicidas [Tesis Magister Scientiae] Facultad de CienciasAgrarias Universidad Nacional de Mar del Plata BalcarceArgentina 2008
[21] J E Gyenge J D Edelstein and C E Salto ldquoEfectos dela temperatura y la dieta en la biologıa de Eriopis connexa(Germar) (Coleoptera Coccinellidae)rdquo Anais da SociedadeEntomologica do Brasil vol 27 no 3 pp 345ndash356 1998
[22] E D Saini and O R de Coll ldquoClave para la identificacion delos coccinelidos (Coleoptera) encontrados en yerba materdquo RIAvol 27 no 2 pp 231ndash241 1996
[23] S Eizaguirre ldquoNueva especie del genero Eriopis (ColeopteraCoccinellidae)rdquo Boletın de la SEA no 35 pp 47ndash49 2004
[24] C S Holling ldquoPrinciples of insect predationrdquoAnnual Review ofEntomology vol 6 pp 163ndash182 1961
[25] E W Evans ldquoSearching and reproductive behaviour offemale aphidophagous ladybirds (Coleoptera Coccinellidae) areviewrdquo European Journal of Entomology vol 100 no 1 pp 1ndash102003
[26] I Bertolaccini P Andrada and O Quaino ldquoEfecto de fran-jas marginales en la atraccion de Coccinellidae y Syrphidaedepredadores de afidos en trigo en la zona central de laprovincia de Santa Fe Argentinardquo Agronomıa Tropical vol 58no 3 pp 267ndash276 2008
[27] J P Harmon A R Ives J E Losey A C Olson and K SRauwald ldquoColeomegilla maculata (Coleoptera Coccinellidae)predation on pea aphids promoted by proximity to dandelionsrdquoOecologia vol 125 no 4 pp 543ndash548 2000
[28] J Lys and W Nentwig ldquoAugmentation of beneficial arthropodsby strip-managementmdash4 Surface activity movements andactivity density of abundant carabid beetles in a cereal fieldrdquoOecologia vol 92 no 3 pp 373ndash382 1992
[29] J A Lys and W Nentwig ldquoImprovement of the overwinter-ing sites for Carabidae Staphylinidae and Araneae by strip-management in a cereal fieldrdquo Pedobiologıa vol 38 no 3 pp238ndash242 1994
[30] D M Carmona and D A Landis ldquoInfluence of refuge habitatsand cover crops on seasonal activity-density of ground beetles(Coleoptera Carabidae) in field cropsrdquoEnvironmental Entomol-ogy vol 28 no 6 pp 1145ndash1153 1999
[31] M Jonsson SDWrattenDA Landis andGMGurr ldquoRecentadvances in conservation biological control of arthropods byarthropodsrdquo Biological Control vol 45 no 2 pp 172ndash175 2008
[32] M M Gardiner D A Landis C Gratton et al ldquoLandscapediversity enhances biological control of an introduced crop pestin the North-Central USArdquo Ecological Applications vol 19 no1 pp 143ndash154 2009
[33] R Isaacs J Tuell A Fiedler M Gardiner and D Landis ldquoMax-imizing arthropod-mediated ecosystem services in agriculturallandscapes the role of native plantsrdquo Frontiers in Ecology andthe Environment vol 7 no 4 pp 196ndash203 2009
[34] K Ma S Hao H Zhao and L Kang ldquoStrip cropping wheatand alfalfa to improve the biological control of the wheataphidMacrosiphumavenae by themiteAllothrombiumovatumrdquoAgriculture Ecosystems and Environment vol 119 no 1-2 pp49ndash52 2007
[35] M P Dıaz and C G Demetrio Introduccion a los ModelosLineales Generalizados Su Aplicacion a las Ciencias BiologicasScreen Edit Cordoba Spain 1998
[36] SAS Institute Inc SASSTAT 92Userrsquos Guide SAS Institute IncCary NC USA 2008 httpsupportsascomdocumentationcdlenstatuggenmod61787PDFdefaultstatuggenmodpdf
[37] A Langer and T Hance ldquoEnhancing parasitism of wheat aphidsthrough apparent competition a tool for biological controlrdquoAgriculture Ecosystems and Environment vol 102 no 2 pp205ndash212 2004
[38] R Beltrame and C Salto ldquoAmmi majus L y Foeniculum vulgareMiller como hospedantes de afidos y sus enemigos naturalesrdquoRevista de la Facultad de Agronomıa Universidad NacionalBuenos Aires vol 20 no 3 pp 395ndash400 2000
[39] A Ferran and A F G Dixon ldquoForaging behaviour of ladybirdlarvae (Coleoptera Coccinellidae)rdquo European Journal of Ento-mology vol 90 no 4 pp 383ndash402 1993
[40] A F G Dixon and Y Guo ldquoEgg and cluster size in ladybirdbeetles (Coleoptera Coccinellidae) the direct and indirecteffects of aphid abundancerdquo European Journal of Entomologyvol 90 pp 457ndash463 1993
[41] J Y Xia W van der Werf and R Rabbinge ldquoTemperatureand prey density on bionomics of Coccinella septempunc-tata (Coleoptera Coccinellidae) feeding on Aphis gossypii(Homoptera Aphididae) on cottonrdquo Environmental Entomol-ogy vol 28 no 2 pp 307ndash314 1999
[42] G J K Griffiths J M Holland A Bailey and M B ThomasldquoEfficacy and economics of shelter habitats for conservationbiological controlrdquo Biological Control vol 45 no 2 pp 200ndash209 2008
[43] J L Hemeptine A F G Dixon J L Doucet and J E PetersenldquoOptimal foraging by hoverflies (Diptera Syrphidae) andladybird (Coleptera Coccinellidae) mechanimismsrdquo EuropeanJournal of Entomology vol 90 pp 451ndash455 1993
[44] F J J A Bianchi and W van der Werf ldquoModel evaluation ofthe function of prey in non-crop habitats for biological controlby ladybeetles in agricultural landscapesrdquo Ecological Modellingvol 171 no 1-2 pp 177ndash193 2004
