The impact of rubber plantations on the diversity and activity of understorey insectivorous bats in...

ORI GIN AL PA PER

The impact of rubber plantations on the diversityand activity of understorey insectivorous batsin southern Thailand

Phansamai Phommexay • Chutamas Satasook • Paul Bates •

Malcolm Pearch • Sara Bumrungsri

Received: 23 December 2009 / Accepted: 17 March 2011 / Published online: 27 March 2011� Springer Science+Business Media B.V. 2011

Abstract Although a large proportion of tropical rain-forest in South-east Asia has been

replaced by rubber plantations, there is very little information about the impact of such

forest conversion on bat diversity. To address this deficiency, trapping and acoustic

monitoring programmes were carried out in Ton Nga Chang and Khao Ban That wildlife

sanctuaries in southern Thailand with the purpose of comparing species diversity and

activity of understorey insectivorous bats at sites in forest and in nearby monoculture

rubber plantations. Insect biomass in both habitats was assessed. Bat species diversity and

activity were found to be much lower in rubber plantations than in forested areas and mean

insect biomass was determined to be more than twice as high in the latter habitat than in the

former. Bats utilising forest were shown to have significantly higher call frequencies

but marginally lower wing loadings and aspect ratios than bats found in both habitats.

Management strategies to increase biodiversity in rubber plantations are discussed.

Keywords Bat activity � Bat diversity � Echolocation call � Feeding buzz �Insect biomass � Rubber plantation � Tropical forest � Wing morphology

P. Phommexay � C. Satasook � S. Bumrungsri (&)Department of Biology, Faculty of Science, Prince of Songkla University,Hat Yai, Songkla 90112, Thailande-mail: [email protected]

P. PhommexayFaculty of Forest, National University of Laos, Vientiane, Lao PDRe-mail: [email protected]

P. Bates � M. PearchHarrison Institute, Centre for Systematics and Biodiversity Research,Bowerwood House, St. Botolph’s Road, Sevenoaks, Kent TN13 3AQ, UKe-mail: [email protected]

123

Biodivers Conserv (2011) 20:1441–1456DOI 10.1007/s10531-011-0036-x

Introduction

Global tropical rain-forest is being lost rapidly owing to various human activities: over the

last decade, 5.8 million ha per year of humid forest have been cleared and an additional 2.3

million ha have been degraded. South-east Asia has a highest annual deforestation rate of

2.5 million ha, of which 1.06 million ha have been converted to agricultural land with the

remainder having been degraded (Achard et al. 2002). At the current rate of deforestation,

about 74% of forest in this region could be lost by the end of this century (Sodhi et al.

2004). In Thailand, forest covered half of the area of the country in 1961 but only 31% in

2006, 18.2% of which comprised nature reserves with protected area status (Trisurat 2007).

A large proportion of primary forest in South-east Asia has been converted into com-

mercial plantations (a so called ‘green desert’) of exotic trees such as rubber (Heveabrasiliensis) and oil palm (Elaeis guineensis). The global area of rubber plantations

doubled between 1960 and 2000 (Aratrakorn et al. 2006). Currently, the global planted area

of rubber is 10.1 million hectares, 75% of which are in South-east Asian countries

(International Rubber Study Group 2008), especially Indonesia, Thailand, and Malaysia. In

Thailand, the rubber tree, which is native to the Amazon rain-forest, was first planted in

1899. The planted area in this country increased four-fold between 1960 and 2005, with the

major increase occurring during the first half of that period (UNCTAD 2010). Thailand,

second after Indonesia in terms of planted area, currently has 2.28 million ha of rubber

plantations (ca. 5% of country’s area and 22.53% of the global rubber area), the majority of

which (ca. 80%) occur in the southern peninsula. Since 1980, when the government

introduced a fund to encourage the planting of new, cloned trees, rubber production in

Thailand has increased sharply. Since 1990, the country has been the largest global

exporter of natural rubber with the commodity generating the highest income for the nation

of any agricultural product (6.57 billion U.S. dollars in 2008) (Office of Agricultural

Economics 2009). In Indonesia and Malaysia, rubber plantations are owned and operated

both by smallholders and by larger estates whilst plantations in Thailand are owned solely

by smallholders. In southern Thailand, which is characterised by a tropical wet seasonal

climate, rubber plantations contributed the same amount of area as forest (25%) in 2006

(Department of National Park, Wildlife and Plant Conservation 2010).

Agricultural intensification and expansion is considered to be the severest threat to

biodiversity (Donald 2004). Rubber, similar to other tropical cash crops (e.g. cacao, oil

palm, coffee), grows generally within areas characterised by high rainfall and low eleva-

tion. Such areas normally support tropical moist forest, one of the most species-rich

terrestrial biomes. Although relatively little research has been undertaken, studies have

shown that rubber and oil palm plantations hold less than half of the vertebrate species that

are known to occur in primary forest (Danielsen and Heegaard 1995; Aratrakorn et al.

2006; Fitzherbert et al. 2008; Fukuda et al. 2009) and that the effect of plantations differs

between groups of invertebrates. Faunal assemblages in plantations tend also to be dom-

inated by a few widespread, generalist, non-forest species and pests (Aratrakorn et al.

2006; Fitzherbert et al. 2008). Such monocultures, however, contain few taxa of conser-

vation significance. In a study on birds in lowland forest in Thailand, all but one of 16

Threatened or Near Threatened species were found only in forest (Aratrakorn et al. 2006).

South-east Asia is one of the world’s bat diversity hotspots. Regionally, it habours 30%

of the known global bat fauna (ca. 320 species) (Kingston 2010). In Thailand, where more

than 119 species are considered to occur (Bumrungsri et al. 2006), bats comprise at least

40% of the mammalian fauna. Bats are regarded as major pollinators of many food plants

in this region, including durian and petai (Bumrungsri et al. 2008, 2009). They also play a

1442 Biodivers Conserv (2011) 20:1441–1456

123

major role in controlling insects in agricultural areas (Leelapaibul et al. 2005). However,

more than 40% of bats in this region are adjudged to be of conservation concern (Kingston

2010). Although no intensive surveys have been carried out, anecdotal information sug-

gests that South-east Asian bat populations are in decline (Mickleburgh et al. 1992;

Bumrungsri et al. 2008), a major cause of which is thought to be the loss or reduction in the

quality of feeding habitats (Racey and Entwistle 2002; Kingston 2010). To date, only two

publications have examined the response of bats to rubber and oil palm plantations

(Danielsen and Heegaard 1995; Fukuda et al. 2009). Both studies show that insectivorous

bats are either extremely rare or absent in these monoculture plantations. Although bats are

considered to be highly agile, which may mitigate the impact on them of these land use

changes, not all species are as mobile as perceived (Struebig et al. 2008). Previous

intensive studies on palaeotropical, insectivorous bat communities in Peninsular Malaysia

and Borneo have indicated that most of the bats captured within the forest interior forage

strictly or predominantly in the highly cluttered space of the forest understorey (Kingston

et al. 2003; Struebig et al. 2006). These ‘narrow space’ bats are particularly susceptible to

habitat destruction owing to their highly specialised wing morphology and echolocation

call design, which may not allow them to forage effectively in the more open habitat found

in plantations. This could lead accordingly to lower bat diversity and feeding activity in

this man-made environment.

The objective of the present study is to compare bat species diversity and feeding

intensity of understorey bats found in forest with species diversity and feeding intensity of

understorey bats found in nearby rubber plantations. Species diversity and activity were

determined primarily by acoustic monitoring, which is an effectual method of sampling

flying bats (Kunz et al. 1996; Barclay 1999; Murray et al. 1999; O’Farrell and Gannon

1999). In addition, a harp trap, which is relatively effective in capturing understorey

insectivorous bats (Tidemann and Woodside 1978; Francis 1989), was also used for bat

sampling. The characters of those insectivorous bat species that could be affected seriously

by the conversion of forest to monoculture rubber plantations are also examined.

Methods

Study area

This study was conducted in southern Thailand in the lowland tropical rain-forest of Ton

Nga Chang Wildlife Sanctuary (WS), Songkhla Province and Khao Ban That WS, Trang

and Phattalung Provinces, and rubber plantations close to them (6–7� N, 99–101� E). The

study was conducted from June to December 2007. The major forest type of the sites

sampled was lowland moist tropical forest with several sampling sites being located

adjacent to limestone hills. Within the forests found in the study area, four canopy layers

were identified: the emergent layer; the top canopy; the middle canopy; and the under-

storey. Forest understorey is characterised mainly by dense saplings of canopy trees,

palms, shrubs, and rattans. Ton Nga Chang WS and Khao Ban That WS cover about 18,195

and 126,696 ha, respectively. The elevation of these areas ranges from 100 to 1,350 m asl.

The average annual temperature is 27.4�C and the average annual rainfall is 2,118 mm in

the former and 2,427 mm in the latter. The rainy season is from May to December and

there is a short dry season from January to March (Bøgh 1996). Generally, rubber plan-

tations cover the vast majority of the areas surrounding these protected forests while

smaller areas of fruit orchards and oil palm plantations are also present.

Biodivers Conserv (2011) 20:1441–1456 1443

123

Sampling design

Twenty-five pairs of forest-rubber plantation sites were sampled. The sampling sites in

intact forest were selected on account of their accessibility. Access to these sites was by

trails or roads. A sampling site in a rubber plantation was selected only if the plantation

was larger than two hectares, the rubber trees were more than 10 years old, and the

plantation had not been sprayed with herbicide within the preceding 2 months. It is usual

for rubber trees in these intensive monoculture plantations to be planted in rows that are

7 m apart with a distance between individual trees of 3 m (stem density = 476 stem/ha). In

the study area, plantations of rubber trees of different ages were usually contiguous, with

no break between younger and older plantations. Few native trees are found within areas of

rubber production since it is the policy of the government’s rubber replanting aid fund to

have intensive monoculture plantations. Herbicide treatment or weeding is undertaken

approximately every 6 months in these plantations with the result that the understorey

remains relatively open. As each site was located within 2 km of its twin (mean ±

SE = 0.74 ± 0.11, range 0.18–1.74 km), it is assumed that sampled bats were from the

same community. A minimum distance of 0.5 km separated each pair of sampling sites

(mean ± SE = 3.49 ± 1.65, range 0.54–29.25 km). Each sampling site was positioned at

least 150 m from the edge of the forest or rubber plantation in order to minimise the

sampling of bats foraging on the periphery of both habitats.

Acoustic studies

Understorey insectivorous bats that are considered to be sensitive to habitat conversion

were sampled acoustically. Bat activity was monitored in both habitats simultaneously

with 109 time expansion ultrasonic bat detectors (Petterson D-240x, Uppsala, Sweden),

each of which was connected to a digital recorder (Sony iRiver, H320). Bat detectors

were secured in boxes 1.2 m above the ground and were angled approximately 15� above

the horizontal plane. The boxes were positioned in forest gaps, on trails, and between the

rows of rubber trees. Detectors were set to capture and record calls above the selected

trigger level automatically with 17 s of playback. The trigger level was set to ‘‘low’’ so

that both high and low frequency calls up to 200 kHz were detected. Acoustic sampling

at all sites was undertaken at the same time each night to take account of any variation

in bat activity caused by fluctuating weather conditions (e.g. rain and/or wind). Echo-

location calls were recorded for 3 h between 18.30 h (5–35 min after sunset) and 21.30 h

following the results of previous studies that suggest that bat activity is greatest during

this period (Bumrungsi et al. unpublished data). Acoustic sampling was not conducted in

heavy rain or during a full moon as bat activity is reduced in these conditions (Weinbeer

and Meyer 2006).

Bat trapping

Although bat activity and species diversity were determined primarily through acoustic

sampling, bats were also secured physically in order for species’ identifications to be

established. The bats were collected in forest areas in four-bank harp traps set across trails

or streams and, in rubber plantations, in a single harp trap and two 2.9 9 12 m mist nets.

Mist nets were not used in forest zones owing to the highly cluttered nature of the un-

derstorey. Trapping and netting were undertaken at each site during or after acoustic


123

sampling. When trapping was carried out on the same night as acoustic monitoring, traps

were set at least 150 m away from the acoustic sampling point. This was done to minimise

any over-representation in bat activity at the acoustic sampling point that may have been

caused by free-flying bats being attracted by the distress calls of netted bats (see Russ et al.

2004). Harp traps and mist nets were checked every 15–20 min until the conclusion of the

trapping session at 21.30 h. The body mass of each bat was measured and echolocation

calls were recorded from hand-held bats. Calls were recorded also from bats after release

as call frequencies of flying bats differ from those at rest. Both readings were used to

establish call references for the species collected. These call references were of assistance

in identifying the same species at the acoustic sampling points. Taxonomic identification of

all species in the hand was based on Corbet and Hill (1992), Bates and Harrison (1997),

Payne et al. (1998), and Francis (2008). For bat species that were unable to be identified in

the field, voucher specimens were taken. These were preserved in 70% alcohol before

being deposited in the Princess Maha Chakri Sirindhorn Natural History Museum, Prince

of Songkla University (PSU) for taxonomic identification.

Wing tracing

Bat wing morphology was examined as it has been shown that there is a relationship

between wing shape and the type of habitat in which particular species forage (Aldridge and

Rautenbach 1987; Norberg and Rayner 1987; Altringham 1996). The right wing of each

collected bat was laid on a sheet of graph paper and photographed with a Fuji S5700 camera.

The following wing morphometrics were measured from the photograph using Photoshop

CS2, version 9: wing area (S), armwing area (Saw) handwing area (Shw), armwing length

(law), and handwing length (lhw). A tpsDig2 programme (tpsSuper-digitised programme)

was used to calculate the wing area. The following characters are used to define the wing

morphometry of bats: (1) Wing loading = Mg/S; (2) Aspect ratio = B2/S; and (3) Wing

shape index = Ts/Tl-Ts where Ts is the ratio of the handwing to the area of the armwing

(Ts = Shw/Saw), Tl is the ratio of handwing length to armwing length (Tl = lhw/law), and

B is the wingspan. All wing definitions follow Aldridge and Rautenbach (1987), Norberg

and Rayner (1987), and Altringham (1996).

Insect sampling

To determine the variation (if any) in insect biomass between habitats, insects were

sampled simultaneously in 12 paired sampling sites in intact forest and in rubber planta-

tions using suction traps. This trap is suitable for sampling small and weakly flying insects

in less windy conditions (Southwood and Henderson 2000), as the breezes in tropical forest

understorey are typically light. Unlike light-sampling, suction traps do not depend upon

physiological responses of the insects. Suction traps were placed 3 m above ground level in

gaps in both habitats with each trap being set at least 50 m from the nearest acoustic

monitoring site. The traps sampled insects for 30 min in the second half of each hour

during a 3 h period (18.30–21.30 h). The captured insects were retained in jars containing

70% alcohol. Insect specimens were identified to Order level following Borror et al. (1989)

before being sorted into 12 size categories based on body length (0.1–2.0, 2.01–4.00,

4.01–6.00 etc. (to 22.01–24.0 mm)). Following Rogers et al. (1976), insect biomass

was estimated as follows: W = 0.0305L2.62 where W is dry mass (mg) and L is body

length (mm).


123

Habitat clutter measurement

Particular bat species are suited to certain types of habitat on account of their wing

morphology, call design, and the level of clutter present. Habitat clutter was determined

qualitatively and quantitatively.

The quality of clutter was determined by creating a vertical stratification profile of one

acoustic sampling site in forest and one in a rubber plantation. A rangefinder was used to

calculate (a) the total height and (b) the height at the first branch of all trees and shrubs that

had a trunk or stem diameter greater than 5 cm and that lay within 30 m of the central point

of each site. The profile of each site was plotted from the data gathered.

Habitat clutter was quantified as the percentage of ‘hits’ in eight sampling sites in each

habitat (Brockelman 1998) (Fig. 4). A 22 m metal pole with marks every two metres was

positioned vertically at one metre intervals along a 10 m line running north, south, east,

and west of the central point of each of the 16 sampling sites. A ‘hit’ is defined as

vegetation touching the pole at any of the eleven 2 m marks.

Sound analysis

Recorded calls were analysed with Bat-Sound Pro 3.1 (Pettersson Elektronik, Sweden).

The number of bat passes and feeding buzzes or terminal buzzes was counted in each 17 s

time frame. A bat pass is defined as an echolocation call with at least two consecutive

pulses (Hayes 1997). A feeding buzz is a distinctive sound indicating a feeding attempt. If

continuous pulses with a similar call character lasted more than 15 min, it was assumed

that the bat was resting; this was treated as a single bat pass. Excepting members of the

Families Rhinolophidae and Hipposideridae, bats were identified to species level by

comparing peak call frequencies, firstly, with call characters detailed in Hughes et al.

(2010); secondly, with the call reference collection established in the present study; and,

thirdly, with the call library of the Bat Research Unit, Prince of Songkla University.

Constant call frequency was used to identify Rhinolophus and Hipposideros species as this

type of call is sufficient to discriminate species of these two genera (Russo and Jones 2002;

Fugui et al. 2004; Hughes et al. 2010). In addition to peak frequency comparisons, the taxa

Emballonura monticola and Taphozous longimanus were able to be identified by their

unique frequency-modulated calls.z

Statistical analysis

A paired sample T-test was used to compare the number of bat passes, feeding

buzzes, and insect biomass occurring in both habitats. Spearman’s correlation test was

used to investigate the relationship between bat passes and insect biomass. A Chi-

square contingency test was used to examine variation between habitats in the bio-

mass of each insect Order. Rarefaction curves were plotted in order to assess the

completeness of bat surveying in both habitats. Mann–Whitney U tests were used to

examine the variation in body mass, call frequency, and wing morphometrics between

bats found in forest and bats found in both rubber plantations and forest. SPSS 14.0

for Windows (SPSS Inc.) was used for all statistical analyses (mean ± SE was used

throughout).


123

Results

Acoustic studies

Equal acoustic sampling of 25 sites in each habitat showed that bat passes, feeding buzzes,

and bat species richness were much higher in forest than in rubber plantations. In total, 377

bat passes and 112 feeding buzzes were recorded in forest while 222 bat passes (58% of

those in forest) and 37 feeding buzzes (33%) were registered in rubber plantations. The

mean number of bat passes in forest (mean ± SE, 15.08 ± 1.72) was significantly higher

than that in rubber plantations (8.88 ± 1.23) (paired sample T-test, t = 2.87, df = 24,

P = 0.008) (Fig. 1). At least 19 species were found acoustically in forest whereas ten

species were recognised in rubber plantations (Table 1).

Fig. 1 Average number of bat passes (a) and average insect biomass (mg.) (b) in 3 h of sampling at 25pairs of sampling sites in forest and rubber plantations. Mean and 95% confidence intervals are shown


123

Bat trapping

As was the case with acoustic sampling, bat species richness and the number of captured

bats were both notably higher in forest than in rubber plantations. In forest, 355 individuals

of 24 insectivorous bat species were captured (Table 1). These bats belonged mainly to the

Families Rhinolophidae and Hipposideridae and included Rhinolophus affinis, R. lepidus,

R. malayanus, R. stheno, R. robinsoni, R. trifoliatus, R. luctus, R. yunanensis, Hipposiderosbicolor, H. diadema, and H. cineraceus. Sixteen individuals of eight insect-eating bat

species (R. affinis, R. luctus, R. stheno, H. bicolor, H. larvatus, Phoniscus jagorii, Mini-opterus magnater and Magaderma spasma) were caught in nearby rubber plantations.

Table 1 Species and number of insectivorous bats captured and recorded at 25 pairs of sampling sites inforest and in rubber plantations

Family Species Forest Rubber plantation

Hipposideridae Hipposideros bicolor 85,x 4,x

Hipposideros cineraceus 4,x

Hipposideros diadema 4,x

Hipposideros armiger X

Hipposideros larvatus 16,x 1,x

Coelops frithii 2,x

Taphozous longimanus x

Emballonura monticola x x

Megadermatidae Megaderma spasma 4 1

Nycteridae Nycteris tragata 1,x

Rhinolophidae Rhinolophus acuminatus 6,x

Rhinolophus affinis 99,x 6,x

Rhinolophus coelophyllus 1,x

Rhinolophus lepidus 29,x x

Rhinolophus luctus 3,x 1,x

Rhinolophus malayanus 13,x

Rhinolophus robinsoni 4,x x

Rhinolophus stheno 32,x 1,x

Rhinolophus trifoliatus 3,x x

Rhinolophus yunanensis 3,x

Vespertilionidae Kerivoula hardwickii 21,x

Kerivoula minuta 3

Miniopterus magnater 7 1

Murina cyclotis 9

Murina suilla 2

Myotis muricola 3

Phoniscus jagorii 1

Pipistrellus cf. tenuis 1

Number of bat species captured 24 8

Number of individuals captured 355 16

Number of species recorded 19 10

Species detected by means of acoustic sampling are indicated by the letter ‘x’


123

From rarefaction curves based on harp trap sampling, no asymptote was reached in either

habitat after 93 h of trapping effort (Fig. 2). Therefore, it appears that a greater number

species could be found in each habitat if more extensive sampling were carried out.

Insect biomass

From 12 paired sampling sites, insect biomass was found to be significantly higher in forest

(mean ± SE, 849.7 ± 184.4 mg) than in rubber plantations (358.5 ± 88.6 mg) (paired

sample T-test, t = 2.85, DF = 12, P = 0.016). Eight insect Orders were found in rubber

plantations (Lepidoptera, Diptera, Coleoptera, Hemiptera, Homoptera, Hymenoptera,

Isoptera and Tricoptera) while ten insect Orders were recorded in forest. The biomass of

Lepidoptera, the greatest contributor, was proportionally significantly higher in forest

(74%) than in rubber plantations (58%) (Chi-square test, Chi-square = 2387.8, df = 4,

P \ 0.001). Diptera were moderately abundant (21–33%) and other insect orders (Cole-

optera, Hemiptera, Homoptera, Hymenoptera, Isoptera, Tricoptera, Orthoptera and Odo-

nata) were relatively rare (1–5%). At any given site, the number of bat passes did not

correlate significantly with insect biomass either in forest (r = 0.127, N = 12, P = 0.695)

or in rubber plantations (r = 0.189, N = 12, P = 0.555).

Habitat clutter

Forest and rubber plantation profiles were markedly different. There was more complexity

and higher tree density in forest than in rubber plantations (Fig. 3). In terms of habitat

clutter, intact forest was found to have the highest clutter in the understorey (2–6 m)

(36.3–46%), intermediate clutter at midstorey (8–18 m) (12–24%), and the least clutter at

canopy level ([20 m) (3.4–5.6%). In contrast, there was significantly less clutter from 0 to

6 m in rubber plantations (0–18%) (t = 7.47, DF = 38, P \ 0.001). The clutter level at

0

5

10

15

20

25

30

35

0 9 18 27 36 45 54 63 72 81 90

Capture effort (Hours)

Cum

ulat

ive

no. s

peci

es(a)

(b)

Fig. 2 Rarefaction curves (solid lines) showing the number of bat species expected from harp-trapping in(a) forests and (b) rubber plantations. Ninety-five percent confidence intervals for forest (dotted line) andrubber plantations (dashed line) are displayed


123

8–18 m in rubber plantations was comparable to forest (7.8–18%) (T = 1.16, DF = 93,

P = 0.24) while the emergent strata over 22 m were absent in rubber plantations (Fig. 4).

Wing morphology

Twenty-five bat species were identified within the study site using acoustic analysis and

direct capture and these were split into three groups: those species recorded in forest; those

recorded in both forest and rubber plantations; and those recorded only in rubber planta-

tions. Thirteen bat species were found in forest (Hipposideros armiger, H. cineraceus,

H. diadema, Coelops frithii, Nycteris tragata, Rhinolophus acuminatus, R. coelophyllus,

R. malayanus, Kerivoula hardwickii, K. minuta, Murina cyclotis, M. suilla, and Myotismuricola); eleven species were recorded in both forest and rubber plantations (Embal-lonura monticola, H. bicolor, H. larvatus, Megaderma spasma, R. affinis, R. lepidus,

R. luctus, R. robinsoni, R. stheno, R. trifoliatus, and Miniopterus magnater); and only one

species (Phoniscus jagorii) was found solely in rubber plantations. Bats recorded in forest

had a marginally lower wing loading (mean ± SE, 6.54 ± 0.67 N/m2, range 4.22–11.88)

and aspect ratio (7.09 ± 0.20, range 5.61–8.18) compared to bats recorded in forest and/or

Fig. 3 The vertical stratification of a 10 9 30 m sampling site in (a) forest and (b) a rubber plantation.Between 10 and 20 m in forest sites, plants with a minimum stem diameter of 5 cm were counted. From 0 to10 m and 20 to 30 m, only plants with a stem diameter greater than 15 cm were included

Fig. 4 The percentage of vegetation ‘‘hits’’ at 2 m vertical intervals (range: 2–22 m) at 40 pole positions in16 sampling sites in forest and rubber plantations. The greater the percentage, the higher the clutter level


123

rubber plantations (including P. jagorii) (wing loading: 7.24 ± 0.49 N/m2, range

4.93–10.47; aspect ratio: 7.74 ± 0.42, range 5.69–10.64). The wing tip index of species in

the former group (2.77 ± 0.39, range 1.12–4.96) was comparable to the wing tip index of

species in the latter group (including P. jagorii) (2.72 ± 0.27, range 1.46–4.15).

Accordingly, wing tip indices were not considered to be statistically significant (P [ 0.05).

Call frequencies of bats recorded in forested areas (mean ± SE, 99.79 ± 6.92 kHz, range

57.8–148.1) were markedly higher than those found in forest and/or rubber plantations

(including P. jagorii) (76.06 ± 8.61 kHz, range 32.1–140.4) (t = 2.16, DF = 23,

P = 0.04).

Discussion

The data gathered would indicate that rubber plantations have a negative impact on

insectivorous bats. The number of bat passes and feeding buzzes recorded in rubber

plantations was significantly (about two to three times) lower than in forest. Similarly,

average insect biomass in rubber plantations was about two times lower than in forest. It

should be borne in mind, however, that the data on which these findings are based were

gathered during a limited sampling period in the earlier hours of the night. It is likely that

sampling undertaken throughout the course of an entire night would produce more con-

clusive data.

The lower insect biomass in rubber plantations may be due to the floristic impover-

ishment of this habitat since insects are mostly herbivores that feed selectively on plants

(Holloway et al. 1992). Further, greater protection from predators is provided by the higher

levels of clutter found in forest understorey (Patriquin and Barclay 2003; Lumsden and

Bennett 2005) than in the relatively clutter-free environment of rubber plantations. In

addition, the stems and leaves of rubber trees are used rarely by insects owing to their

toxicity although some groups of insects are known to pollinate the flowers of rubber trees

(Thapa 2006). It is also unlikely that the lower insect biomass in rubber plantations

reported in the present study is a result of the use of pesticides as these are not employed

regularly owing to the low incidence of insects in these areas.

The correlation of bat activity to insect biomass suggests that higher bat activity in

forest reflects greater insect availability in this habitat. Previous studies have indicated that

bat activity increases as prey availability increases (Agosta et al. 2003; Bartonicka and

Rehak 2004; Lang et al. 2006) and that bats select foraging sites based partially on insect

availability. In the present study, the spatial range of bat activity is likely to be limited

principally to the understorey and middle canopy as the bat detection microphone was set

at understorey level. Since forest understorey is much denser than the understorey in rubber

plantations, bat activity in forested areas could be under-represented to a greater degree

than that in rubber plantations.

The greater abundance and species richness of bats in forest sites compared to rubber

plantations was also indicated by the results of direct trapping. It should be noted, however,

that trapping methods employed in the two habitats were not uniform owing to the dif-

ferences in habitat character (i.e. mist nets were not used in forest). The species diversity

determined by direct capture should be treated with caution. Harp trapping is less effective

in the relatively open areas of rubber plantations as it samples only a small area of the site.

The positioning of harp traps across streams or trails in forest is much more effective as

sampling is concentrated on flyways that bats use regularly (when commuting between

feeding areas, for example). Although mistnets were used only in rubber plantations, bat


123

species in this habitat are probably under-represented as insectivorous bats are known to

avoid mistnets (Francis 1989, MacCarthy et al. 2006, Larsen et al. 2007).

In addition to insect availability, the greater incidence of bat species in forest may be

explained in terms of the heterogeneity of microhabitats that support species with varying

wing morphology and call frequencies. Although the forest understorey is more cluttered

compared to that of rubber plantations, gaps of various sizes are common (Chandrashekara

and Ramakrishnan 1994), creating a more complex habitat. Similarly, although the clutter

of the top canopy in both habitats is comparable, the emergent strata are present only in

forest, which has, accordingly, a greater canopy complexity (Zurita et al. 2006). Conse-

quently, forest can habour bats that fly generally in gaps as well as those species that forage

in highly cluttered space, whereas the more open and more homogenous understory in

rubber plantations supports mainly bats that fly customarily in gaps. In the present study,

bats occurring in forest were found generally to have lower wing loadings and lower aspect

ratios compared to those found in both forest and rubber plantations. Bat species with a low

wing loading and low aspect ratio are highly manoeuvrable and are able to navigate

cluttered space without difficulty, albeit at low speed (Norberg 1998; Altringham 1996).

Echolocation also has a bearing on the foraging habitat used by bats. Species found in

forest have high call frequencies with low intensity to obviate excessive clutter echoes

(Schnitzler and Kalko 2001). However, such calls are prone to atmospheric attenuation and

the operational range is thus limited. In contrast, bats foraging in more open spaces, such as

rubber plantations, emit calls with lower peak frequencies that are accompanied usually by

a high sound pressure level (Schnitzler and Kalko 2001). Species with low frequency but

high intensity calls are better at detecting echoes from distant targets than species using

low intensity calls, since they are less attenuated (Fenton 1983). Given that insect avail-

ability in monoculture rubber plantations is much lower than in forest, monoculture rubber

plantations are not the optimum habitat for most insectivorous bats, although their wing

morphology may allow them to forage there.

In an earlier study, seven individuals of two fruit bat species (Cynopterus spp.) were

netted in the understorey of rubber plantations (502 net-metre nights) whereas no insec-

tivorous bats were collected (Danielsen and Heegaard 1995). The non-collection of

insectivorous bats may, however, reflect simply the ability of these bats to detect and avoid

mistnets (Francis 1989; Berry et al. 2004; MacCarthy et al. 2006; Larsen et al. 2007),

especially when nets were set in the relatively open habitat of the plantations. Fruit bats

were also common at the plantation sites in this project with 171 bats representing eight

frugivorous species being netted at such sites (1800 net-metre hours) (Phommexay 2009).

Conservation remarks

Currently, there is great concern about the detrimental effect that oil palm and rubber

plantations are having on biodiversity in the tropical forests of South-east Asia (Aratrakorn

et al. 2006; Fitzherbert et al. 2008; Koh and Wilcove 2008; Koh 2008; Wilcove and Koh

2010). Although studies are limited, previous investigations have shown that faunal bio-

diversity is reduced considerably in oil palm and rubber plantations, especially in respect

of forest species, species with small ranges, and taxa of conservation importance

(Aratrakorn et al. 2006; Fitzherbert et al. 2008). In Peninsular Malaysia, it has been shown

that rubber plantations habour only 24% of primary forest birds (Peh et al. 2006).

Although nearly half of all insectivorous bat species documented in the present study

were recorded in rubber plantations, this does not mean to say that these plantations

provide suitable foraging habitat or that they would be able to sustain insectivorous bat


123

diversity over a prolongued period. The bat and insect species recorded in plantations

probably include many individuals that simply have spilled over from large, adjacent tracts

of primary forest since most of the plantations where studies took place are situated within

a kilometre of the latter habitat. To reduce the incidence of such boundary infringements, it

is recommended that further sampling in rubber plantations be undertaken at a greater

distance from the forest edge.

In terms of conservation, compared to other monoculture crops (e.g. oil palm, coffee,

rice, cassava, and sugar cane), rubber plantations may be less detrimental to biodiversity as

they retain a reasonably complex canopy and the period of rotation is long (more than

25 years). Peh et al. (2006) suggest that rubber plantations are more attractive to forest

birds than other types of cultivated land, including oil palm plantations. Although it is clear

that rubber plantations cannot support the level of biodiversity found in primary forest,

they can be effective as corridors between forest patches and as buffer zones around

protected areas. Used in this way, they can be useful in enhancing the movement of

animals in fragmented landscapes. Biodiversity may be increased in rubber plantations if

the ecological and economic management methods employed in other monoculture plan-

tations are followed (see Hartley 2002; Fisher et al. 2006). For instance, mature native trees

should be retained at intervals throughout the plantation as should native understorey

vegetation, which is often the best guage of animal diversity within a given area.

Undergrowth is known to attract a variety of bird species (Peh et al. 2006) and previous

studies have shown that bird species richness is markedly greater in rubber plantations that

retain an understorey and a shrub layer (Aratrakorn et al. 2006). In addition, vegetation at

the edge of rubber plantations and around water bodies should be left intact as these areas

provide a refuge or feeding habitat for many animals, including insects and insectivorous

bats.

Agroforest rubber plantations, which support not only rubber trees but also forest

vegetation and edible and useful plants, are the best alternative to monoculture rubber

plantations as they represent a compromise between economic and sustainable use of

natural resources that lends itself more readily to biodiversity conservation. Introducing

mixed, shade-tolerant tree species with different light requirements, especially nitrogen-

fixing plants, to the spaces between rows of rubber trees can also be an advantage. These

trees increase litter fall and nutrient recycling and decelerate soil erosion (Khanna 1997;

Forrester et al. 2004). Previous studies have indicated that the multi-storeyed cropping of

forest trees and/or fruit plants (e.g. Azadirachta excelsa, Swietenia macrophylla, Shorearoxburghii, Lansium domesticum, Salacca edulis) in rubber plantations does not have a

negative effect on young rubber tree growth (Buranatham et al. 1998; Chukamnerd et al.

1998; Kongsiphan et al. 1998). Further research is needed into the ecological and economic

differences between agroforest rubber plantations and monoculture rubber plantations,

particularly in terms of long term rubber tree growth and rubber yields. In Indonesia,

studies of rubber production in areas of jungle have shown that agroforests, although their

species’ richness cannot be compared with that of intact primary forest, provide a refuge

for biodiversity in deforested landscapes (Thiollay 1995; Beukema and Van Noordwijk

2004; Beukema et al. 2007). In order to balance the habitat requirements of indigenous

fauna with the economic benefits of rubber production, it is suggested that strategies be

implemented in plantations that enhance biodiversity conservation while preserving the

economic value of the rubber crop.

Acknowledgments We are grateful to the staff of Ton Nga Chang WS and Khao Ban That WS, Thailandfor their co-operation. We would like to thank Ariya Dejtaradol, Tuanjit Srithongchuay, Bounsavane


123

Doungbouppha, Phouthone Kingsada, Pipat Soisook, Neil Furey, and all students at the Bat Research Unit,Department of Biology, Prince of Songkla University for their advice and help with fieldwork. Finally, weare most grateful to the Darwin Initiative, DEFRA (Project nos. 14-011 and 18-002), the Harrison Institute,Bat Conservation International (BCI), The Biodiversity Research and Training Program (BRT), and theGraduate School, Prince of Songkla University for their financial support. Thanks are due also to the threeanonymous reviewers, whose comments led to a significant improvement of the original manuscript.

References

Achard F, Eva HD, Stibig H-J, Mayaux P, Gallego J, Richards T, Malingreau J-P (2002) Determination ofdeforestation rates of the world humid tropical forests. Science 297:999–1002

Agosta SJ, Morton D, Kuhn KM (2003) Feeding ecology of bat Eptesicus fuscus: ‘preferred’ prey abundanceas one factor influencing prey selection and diet breadth. J Zool 260:169–177

Aldridge HDJN, Rautenbach IL (1987) Morphology, echolocation and resource partitioning in insectivorousbats. J Anim Ecol 56:763–778

Altringham JD (1996) Bats: biology and behaviour. Oxford University Press, OxfordAratrakorn S, Thunhikorn S, Donald PF (2006) Changes in bird communities following conversion of

lowland forest to oil palm and rubber plantations in southern Thailand. Bird Conserv Int 16:71–82Barclay RMR (1999) Bats are not birds: a cautionary note on using echolocation calls to identify bats: a

comment. J Mammal 80:290–296Bartonicka T, Rehak Z (2004) Flight activity and habitat use of Pipistrellus pygmaeus in a floodplain forest.

Mammalia 68:365–375Bates PJJ, Harrison DL (1997) The bats of the Indian Subcontinent. Harrison Zoological Museum Publi-

cations, Sevenoaks, UKBerry N, O’Connor W, Holderied MW, Jones G (2004) Detection and avoidance of harp traps by echo-

locating bats. Acta Chiropterol 6:335–346Beukema H, Van Noordwijk M (2004) Terrestrial pteridophytes as indicators of a forest-like environment in

rubber production systems in the lowlands of Jambi, Sumatra. Agric Ecosyst Environ 104:63–73Beukema H, Danielsen F, Vincent G, Hardiwinoto S, van Andel J (2007) Plant and bird diversity in rubber

agroforests in the lowlands of Sumatra, Indonesia. Agrofor Syst 70:217–242Bøgh A (1996) Abundance and growth of rattans in Khao Chong National Park, Thailand. For Ecol Manag

84:71–80Borror DJ, Triplehorn CA, Johnson NF (1989) An introduction to the study of insects, 6th edn. Saunders

College Publishing, PhiladelphiaBrockelman WY (1998) Study of tropical forest canopy height and cover using a point-intercept method. In:

Dallmeier F, Comisky JA (eds) Forest biodiversity research, monitoring and modeling: conceptualbackground and Old World case studies. Man and biosphere series, vol 20. UNESCO, Paris,pp 521–531

Bumrungsri S, Harrison DL, Satasook C, Prajukjitr A, Thong-Aree S, Bates P (2006) A review of batresearch in Thailand with eight new species records for the country. Acta Chiropterol 8:325–359

Bumrungsri S, Harbit A, Benzie C, Carmouche K, Sridith K, Racey PA (2008) The pollination ecology oftwo species of Parkia in southern Thailand. J Trop Ecol 24:467–475

Bumrungsri S, Sripaoraya E, Chongsiri T, Sridith K, Racey PA (2009) The pollination ecology of durian(Durio zibethinus, Bombacaceae) in southern Thailand. J Trop Ecol 25:85–92

Buranatham W, Bumrungwong P, Chukamnerd S (1998) Spacing of Mahogany, Sadao Thiem and Payomwhich planting as multicrop in sloping area of rubber Plantation. Songkhla Rubber Research Station,Songkhla. Thailand. (in Thai)

Chandrashekara UM, Ramakrishnan PS (1994) Vegetation and gap dynamics of a tropical wet evergreenforest in the western Ghats of Kerala, India. J Trop Ecol 10:337–354

Chukamnerd S, Buranatham W, Kongsiphan S (1998) Study on planting of rattan and Azadirachta excelsaas multi-storey with Hevea. Songkhla Rubber Research Station, Songkhla. Thailand. (in Thai)

Corbet GB, Hill JE (1992) The mammals of the Indomalayan Region. Natural History Museum Press,Oxford

Danielsen F, Heegaard M (1995) Impact of logging and plantation development on species diversity: a casestudy from Sumatra. In: Sandbukt Ø (ed) Management of Tropical Forests: toward an integratedperspective. Center for Development and Environment, University of Oslo, Oslo, pp 73–92

Department of National Park, Wildlife and Plant Conservation (2010) Statistical data of national park,wildlife and plant conservation. http://www.dnp.go.th/statistics/dnpstatmain.asp. Cited 21 Feb 2011


123

http://www.dnp.go.th/statistics/dnpstatmain.asp

Donald F (2004) Biodiversity impacts of some agricultural commodity production systems. Conserv Biol18:17–37

Fenton MB (1983) Just bats. University of Toronto Press, TorontoFisher J, Lindenmayor DB, Manning AD (2006) Biodiversity, ecosystem function, and resilience: ten

guiding principles for commodity production landscapes. Front Ecol Environ 4:80–86Fitzherbert EB, Struebig MJ, Morel A, Danielsen F, Bruhl CA, Donald PF, Phalan B (2008) How will oil

palm expansion affect biodiversity? Trends Ecol Evol 23:538–545Forrester DI, Bauhus J, Khanna PK (2004) Growth dynamics in a mixed-species plantation of Eucalyptus

globulus and Acacia mearnsii. For Ecol Manag 193:81–95Francis CM (1989) A comparison of mist nets and two designs of harp traps for capturing bats. J Mammal

70:865–870Francis CM (2008) Mammals of Thailand and South-East Asia. Asia Books, BangkokFugui D, Agetsuma N, Hill DA (2004) Acoustic identification of eight species of bat (Mammalia:

Chiroptera) inhabiting forests of southern Hokkaido, Japan: potential for conservation monitoring.Zool Sci 21:947–955

Fukuda D, Taisen OB, Momose K, Sakai S (2009) Bat diversity in the vegetation mosaic around a lowlanddipterocarp forest of Borneo. Raffles B Zool 57:213–221

Hartley M (2002) Rationale and methods for conserving biodiversity in plantation forests. For Ecol Manag155:81–95

Hayes JP (1997) Temporal variation in activity of bats and the design of echolocation monitoring studies.J Mammal 78:514–524

Holloway JD, Kirk-Spriggs AH, Khen CheyVun (1992) The response of some rain-forest insects group tologging and conversion to plantation. Phil Tran R Soc Lond 335:425–436

Hughes AC, Satasook C, Bates PJJ, Soisook P, Sritongchuay T, Bumrungsri S (2010) Echolocation callanalysis and presence-only modelling as conservation monitoring tools for Rhinolophoid Bats inThailand. Acta Chiropterol 12:311–327

International Rubber Study Group (2008) IRSG Rubber Statistical Bulletin 62(3) November/DecemberKhanna PK (1997) Comparison of growth and nutrition of young monocultures and mixed stand of

Eucalyptus globules and Acacia mearnsii. For Ecol Manag 94:105–113Kingston T (2010) Research priorities for bat conservation in Southeast Asia: a concensus approach.

Biodivers Conserv 19:471–484Kingston T, Francis CM, Akbar Z, Kunz TH (2003) Species richness in an insectivorous bat assemblage

from Malaysia. J Trop Ecol 19:67–79Koh LP (2008) Can oil palm plantations be made more hospitable for forest butterflies and birds? J Appl

Ecol 45:1002–1009Koh LP, Wilcove DS (2008) Is oil palm agriculture really destroying tropical biodiversity? Conserv Lett

1:60–64Kongsiphan S, Buranatham W, Chukamnerd S (1998) Planting fruit crops and forest tree as multi storeyed

cropping with Hevea. Songkhla Rubber Research Station, Songkhla. Thailand. (in Thai)Kunz TH, Thomas DW, Richards GC, Tidemann CR, Pierson ED, Racey PA (1996) Observational tech-

niques for bats. In: Wilson DE, Cole ER, Nichols JD, Rudran R, Foster MS (eds) Measuring andmonitoring biological diversity: standard methods of mammals. Smithsonian Institution Press,Washington, DC, pp 105–114

Lang AB, Kalko EK V, Romer H, Bockholdt C, Dechmann DKN (2006) Activity levels of bats and katydidsin relation to the lunar cycle. Oecologia 146:659–666

Larsen RJ, Boegler KA, Genoways HH, Masefield WP, Kirsch RA, Pedersen SC (2007) Mistnetting bias,species accumulation curves, and the rediscovery of two bats on Montserrat (Lesser Antilles). ActaChiropterol 9:423–435

Leelapaibul W, Bumrungsri S, Pattanawiboon A (2005) Diet of wrinkle-lipped free-tailed bat (Tadaridaplicata Buchannan, 1800) in central Thailand: insectivorous bats potentially act as biological pestcontrol agents. Acta Chiropterol 7:111–119

Lumsden LF, Bennett AF (2005) Scattered trees in rural landscapes: foraging habitat for insectivorous batsin South Eastern Australia. Biol Conserv 122:205–222

MacCarthy KA, Carter TC, Steffen BJ, Feldhamer GA (2006) Efficacy of mistnet protocol for the Indianabats: a video analysis. Northeastern Nat 13:25–28

Mickleburgh SP, Huston AM, Racey PA (1992) Old World fruit bats—an action plan for their conservation.IUCN, Gland, p 256

Murray KL, Britzke ER, Hadley BM, Robbins LW (1999) Surveying bat communities: a comparisonbetween mist nets and AnaBat II bat detector system. Acta Chiropterol 1:105–112


123

Norberg UM (1998) Morphological adaptations for flight in bats. In: Kunz TH, Racey PA (eds) Bat biologyand conservation. Smithsonian Institution Press, Washington and London, pp 93–108

Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bat (Mammalia; Chiroptera): wingadaptation, flight performance, foraging strategy and Echolocation. Philos T Roy Soc B 316:335–427

O’Farrell MJ, Gannon WL (1999) A comparison of acoustics versus capture techniques for the inventory ofbats. J Mammal 80:24–30

Office of Agricultural Economics (2009) Commodity. Ministry of Agriculture and Cooperatives. Bangkok,Thailand. http://www.oae.go.th/download/document/commodity.pdf. Cited 20 Feb 2010

Patriquin KJ, Barclay RBM (2003) Foraging by bats in cleaned, thinned and unharvested boreal forest.J Appl Ecol 40:646–657

Payne J, Francis CM, Phillipps K (1998) A field guide to the mammals of Borneo. The Sabah Society,Malaysia

Peh KSH, Sodhi NS, de Jong J, Sekercioglu CH, Yap CAM, Lim SLH (2006) Conservation value ofdegraded habitats for forest birds in southern peninsular Malaysia. Divers Distrib 12:572–581

Phommexay P (2009) Bat species diversity and feeding intensity in intact forest and rubber plantation insouthern Thailand. MSc thesis, Prince of Songkhla University, Thailand

Racey PA, Entwistle AC (2002) Conservation ecology of bats. In: Kunz TH, Fenton MB (eds) Bat ecology.The University of Chicago Press, USA, pp 673–680

Rogers LE, Hinds WT, Buschbom RL (1976) A general weight vs. length relationship for insects. AnnEntomol Soc Am 69:387–389

Russ JM, Jones G, Mackie IJ, Racey PA (2004) Interspecific responses to distress calls in bats (Chiroptera:Vespertilionidae): a function for convergence in call design? Anim Behav 67:1005–1014

Russo D, Jones G (2002) Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy byanalysis of time-expanded recordings of echolocation calls. J Zool 258:91–103

Schnitzler HU, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569Sodhi NS, Koh LP, Brook BW, Ng PKL (2004) Southeast Asian biodiversity: an impending disaster. Trends

Ecol Evol 19:654–660Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Japan, p 575Struebig MJ, Galdigas BMF, Suatma (2006) Bat diversity of the oligotrophic forests of southern Borneo.

Oryx 40:1–13Struebig MJ, Kingston T, Zubaid A, Modh-Adnan A, Rossiter SJ (2008) Conservation value of forest

fragments to Paleotropical bats. Biol Conserv 141:2112–2126Thapa RB (2006) Honeybees and other insect pollinators of cultivated: a review. J Inst Agric Anim Sci

27:1–23Thiollay JM (1995) The role of traditional agroforests in the conservation of rain-forest bird diversity in

Sumatra. Conserv Biol 9:335–353Tidemann CR, Woodside DP (1978) A collapsible bat trap and a comparison of results obtained with the

trap and with mist-nets. Aust Wildl Res 5:355–362Trisurat Y (2007) Applying gap analysis and a comparison index to evaluate protected areas in Thailand.

Environ Manag 39:235–245UNTAD (2010) Information on rubber. http://www.unctad.org/inforcomm/anglais/rubber/sitemap.htm.

Accessed 10 Aug 2010Weinbeer M, Meyer CFJ (2006) Activity pattern of the Trawling Phyllostomid bat, Macrophyllum

macrophyllum, in Panama. Biotropica 38:69–76Wilcove DS, Koh LP (2010) Addressing the threats to biodiversity from oil-palm agriculture. Biodivers

Conserv 19:99–1007Zurita GA, Rey N, Varela DM, Villagra M, Bellocq MI (2006) Conversion of the Atlantic Forest into native

and exotic tree plantations: effects on bird communities from the local and regional perspectives. ForEcol Manag 235:164–173


123

http://www.oae.go.th/download/document/commodity.pdf

http://www.unctad.org/inforcomm/anglais/rubber/sitemap.htm

Date post:	20-Feb-2023
Category:	Documents
Upload:	psu
View:	0 times
Download:	0 times

The impact of rubber plantations on the diversity and activity of understorey insectivorous bats in...

Documents