Abstract Tropical forest gaps are ephemeral and patchi-ly distributed within forest areas and have very differentlight environments compared with closed-canopy forest.We used fruit-baited traps to investigate if gaps are ex-ploited by more opportunistic butterfly species comparedwith closed-canopy forest. Gaps supported a higher di-versity of butterflies in terms of species evenness butclosed-canopy sites contained species with more restrict-ed geographical distributions. There was little similaritybetween the assemblages of butterflies trapped in thecanopy and those in either gap or closed-canopy sites,but the greater similarity was with gaps, and increaseddiversity in gaps was partly due to canopy species turn-ing up in gaps. Dispersal rates (as measured by recapturerates) were higher in gaps and there was evidence thatbutterflies in gaps had relatively larger and broader tho-raxes, indicating a flight morphology adapted for fasterflight. These results support the notion of a distinctivegap fauna comprising more widespread, mobile species.Habitat modification that opens up the canopy is likelyto result in an increase in these widespread species and adecline in understorey species with restricted distribu-tions.

Keywords Dispersal · Flight morphology · Gap dynamics · Borneo · Vertical stratification

Introduction

Lowland tropical rainforest is a complex and dynamicecosystem whose structure and function is affected bynumerous biotic and abiotic factors (Whitmore 1984,1991). One of the major abiotic factors is the amount oflight entering the forest, and this is determined primarilyby canopy cover. Changes in canopy cover and the for-mation of gaps are brought about by tree falls, and tropi-cal forests naturally exist as dynamic mosaics of gaps,areas of regeneration and mature forest (Whitmore1991).The potential role of gap dynamics in determiningplant species richness through effects of light on plantgrowth and survival has received much attention (Denslow 1987; Brokaw and Busing 2000). However,impacts of gap dynamics on other taxa have been lessstudied (Blau 1980; Schemske and Brokaw 1981; Levey1988). Most studies on insects have been directed to-wards understanding impacts of herbivory on plant di-versity under different light regimes (Coley and Barone1996; Brown et al. 1999) and there have been few stud-ies investigating the role of gaps in determining insectcommunity structure and diversity (Spitzer et al. 1997;Feener and Schupp 1998). This is surprising given thatone of the primary impacts of anthropogenic modifica-tion of tropical forests, through such activities as shiftingagriculture and selective logging, is to open up the can-opy.

Light is important in determining the vertical stratifi-cation of butterflies within tropical forests from groundto canopy levels; different light levels above and belowthe canopy maintain highly distinctive canopy and understorey assemblages (DeVries 1988; Burd 1994; DeVries et al. 1997, 1999; Schulze and Fiedler 1998;Schulze et al., in press). Butterflies are also sensitive tolight gradients at ground level (Brown and Hutchings1997; Sparrow et al. 1994) and there is some evidencefor increased butterfly diversity in gaps compared withdense forest (Spitzer et al. 1997). This is predicted by the intermediate disturbance hypothesis (Horn 1975;Connell 1978) and may be due to butterfly assemblages

J.K. Hill (✉ ) · K.C. Hamer · J. Tangah · M. DawoodCentre for Tropical Ecology, Department of Biological Sciences, University of Durham, Durham DH1 3LE, UKe-mail: J.K.Hill@Durham.ac.ukTel.: +44-191-3747079, Fax: +44-191-3742417

J. TangahForest Research Centre, P.O. Box 1407, 90715 Sandakan, Sabah, Malaysia

M. DawoodInstitute for Tropical Biology and Conservation, Universiti Malaysia Sabah, P.O. Box 2073, 88999 Kota Kinabalu, Sabah, Malaysia

Oecologia (2001) 128:294–302DOI 10.1007/s004420100651

J. K. Hill · K. C. Hamer · J. Tangah · M. Dawood

Ecology of tropical butterflies in rainforest gaps

Received: 13 July 2000 / Accepted: 22 January 2001 / Published online: 11 May 2001© Springer-Verlag 2001

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in gaps being supplemented by light-loving canopy spe-cies at ground level. There is some anecdotal evidence insupport of this, but direct comparisons of gap and cano-py faunas have not been carried out.

Measures of local diversity are widely used to investi-gate impacts of habitat disturbance but they give no in-formation on the composition of the butterfly fauna or itsconservation value (Thomas 1991; Hill et al. 1995). Giv-en the patchy and ephemeral nature of gaps, they arelikely to be exploited by opportunistic species and spe-cies dependent on early successional habitats; such spe-cies are likely to have wide geographical distributions(Thomas 1991; Spitzer et al. 1997). Opportunistic spe-cies are also likely to have increased investment in flightrather than reproduction. For example, insects in habitatsthat are patchily distributed and/or ephemeral have beenshown to be more dispersive compared with insects inmore predictable habitats (Dingle 1986; Leslie 1990;Wilson and Gatehouse 1993; Taylor and Merriam 1995;Denno et al 1996; Berwaerts et al. 1998; Hill et al.1999). Forest gaps are scattered throughout areas ofclosed-canopy forest, and differences in the spatial distri-bution of gaps versus intact forest may select for differ-ences in dispersal ability in species occupying these dif-ferent habitats, but this has not been studied.

In this paper we test the hypotheses that forest gapshave higher butterfly diversity than dense closed-canopyforest, and that butterfly assemblages in gaps are moresimilar to the canopy fauna than are those in denseclosed-canopy forest. We also investigate if changes indiversity in gaps are associated with the loss of specieswith restricted distributions. We test the hypothesis thatbutterflies in gaps have higher dispersal rates by measur-ing recapture rates. Insect dispersal ability has been re-lated to adult morphology (Palmer and Dingle 1989;Fairbairn and Roff 1990) and so we also investigate dif-ferences in dispersal ability in terms of relative invest-ment in flight (thorax and wing size and shape) versusreproduction (abdomen size) of butterflies in gaps andclosed-canopy forest.

Materials and methods

Study site

Fieldwork took place at Danum Valley Field Centre, Sabah (Ma-laysian Borneo; 5°N, 117°50′E), The study area lies within theDanum Valley Conservation Area which is a 428-km2 area of un-logged lowland evergreen rain forest (details of site in Marsh andGreer 1992) surrounded by extensive areas of production forest.Temperature (annual mean=26.7°C) and rainfall (annual mean=2822 mm) at the study area are typical of the moist tropics, withlittle monthly variation (Marsh and Greer 1992).

Traps

It is difficult reliably to identify butterflies in the canopy whenthey are in flight, particularly in highly diverse areas such as Bor-neo (Walpole and Sheldon 1999), or to catch these species usinghand nets. Accordingly, this study focused on the guild of fruit-

feeding nymphalid butterflies which can be caught in traps baitedwith rotting fruit. Butterflies can be broadly divided into twoguilds depending on whether adults feed on fruit or nectar, and ap-proximately 75% of nymphalid species recorded on Borneo feedon fruit. In this study, nymphalid butterflies were sampled usingtraps baited with rotting banana (see DeVries 1987 for details oftrap design). Traps were placed in forest gaps (n=4 gaps) and un-der dense, intact canopy (n=4 “shade” locations) between 1–2 mfrom the ground. The forest gaps were formed by natural treefalls,were at least 10 m by 10 m in size and received full sun at midday.Average canopy openness (measured using a spherical densiome-ter; Lemmon 1957) was 16% in gaps compared with <1% in shad-ed sites. Traps were also hung from tree platforms at heights of2 m (n=2 low traps), 20 m (n=2 medium traps) and 40 m (n=2high traps) from the ground. Two fresh bananas were placed ineach trap on the day prior to the first sampling day, and were leftin the trap for the rest of the sample period; a fresh piece of ba-nana was added to each trap every second day. This ensured thatall traps contained a mixture from fresh to well-rotted bait. Thegap and shade traps were >50 m apart and were 200–300 m fromthe platform traps.

Traps were emptied daily (except on a few days when it rainedall day) between 1500 and 1700 hours, and all trapped butterflieswere identified (following Otsuka 1988), marked with a felt-tipped pen and released. No attempt was made to identify individ-uals of the genera Euthalia or Tanaecia as this can be done reli-ably only from the male genitalia, and so all analyses excludethese individuals. There were three study periods; 5 September–2 October 1998, 6 March–19 April 1999, and 25 March–19 April2000. The tree platform traps were operated over slightly moredays in 1998 (5 extra days) and 1999 (13 extra days) than thegap/shade traps, but otherwise all traps were operated concurrent-ly. Thus, the gap and shade traps were checked on 68 days, and thetree platform traps were checked on 86 days, resulting in a total of1,060 trap days. All species sampled in traps were ranked accord-ing to their geographical distribution using distribution data fromTsukada (1982). The two endemic species (Mycalesis kina andStibochiona schoenbergi) were assigned the highest rank (rank=1)and the most widespread species, Melanitis leda (which occurs inthe Oriental, African and Australasian regions), had the lowestrank (rank=54). Species ranked 3–17 had distributions withinSundaland, and species ranked lower than 17 additionally oc-curred in parts of the Oriental and/or Australasian regions (Appen-dix 1).

Diversity measures

We estimated diversity in terms of species richness and evenness,as well as using the Shannon-Wiener index, which combines rich-ness and abundance into a single measure (Magurran 1988). In ad-dition to the total number of species trapped, we estimated speciesrichness using rarefaction (Heck et al. 1975). We estimated spe-cies evenness using Simpson’s index and bootstrap methods wereused to calculate 95% confidence intervals for Simpson’s andShannon-Wiener’s indices. In order to test for differences in diver-sity between traps, pair-wise randomisation tests were carried outbased on 10,000 re-samples of species abundance data followingSolow (1993).

Flight morphology measurements

During the sampling period in 2000, all trapped butterflies weremeasured before being released. Not all species seen during theentire study were trapped in 2000, and so the analyses of bodyflight morphology were not carried out on the complete speciesassemblage sampled during the study. Up to ten individuals weremeasured for any species and sex. The following measurementswere taken by J.K.H. using Vernier callipers to an accuracy of0.1 mm; body length, thorax length and width, abdomen lengthand width, forewing length (wing base to apex) and breadth (mini-

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mum distance between tornus and costa). These variables werethen used to calculate four variables; thorax and abdomen volumes(length×width2), thorax shape (thorax width/length) and wingshape (wing length/breadth). In butterflies, flight speed is positive-ly correlated with wing span (Dudley 1990), thorax mass (princi-pally flight muscle mass; Srygley and Chai 1990) and thoraxwidth (Dempster et al. 1976; Chai and Srygley 1990). The ratio ofwing span to thorax mass has also been related to flight speed andmetabolic rate (Hall and Willmott 2000) while relative abdomenmass (containing reproductive organs, as well as storage organsand haemolymph) is negatively related to flight speed (Srygleyand Chai 1990). Thus thorax and wing measurements in this studyare likely to reflect investment in flight, while abdomen measuresreflect investment in reproduction. All variables were log10 trans-formed for analysis. Mean values were calculated for males andfemales of each species. All variables except for thorax shapewere related to body size (body length), and to account for this al-lometry, data were analysed by ANCOVA with body length as acovariate. All analyses were weighted by sample size and, unlessotherwise stated, sub-family (Nymphalinae, Charaxinae, Satyrinaeor Morphinae) and sex were included as co-factors in ANCOVAs.Only significant results are presented.

Results

Diversity

We caught a total of 951 individuals from 54 species(Appendix 1; excluding Euthalia/Tanaecia individuals).The largest numbers of species were caught in theground-level traps (shade, gap and low; n=34 to 36 spe-cies), compared with the medium (n=19) or high (n=10)traps. Comparison of diversity in traps at ground level showed that species richness was similar among traps (rarefaction estimate 31.8–35.5 species) but thatSimpson’s index (species evenness) was highest in gapscompared with shade and low traps (Table 1; gaps versusshade randomisation test, ∆=4.74, P=0.01). The shadetraps were dominated numerically by one species (Neor-ina lowii) which accounted for >20% of individualscaught (Fig. 1). The Shannon-Wiener estimate of diversi-

ty was significantly higher in the ground-level traps thanthe upper-level traps (Table 1; low versus medium-leveltraps randomisation test, ∆=0.42, P=0.03). The rate ofspecies accumulation was similarly high among the dif-ferent ground-level traps (ANCOVA on log10-trans-formed data using average accumulation curves, eachcurve was based on 20 randomly shuffled samples ofspecies accumulation data to remove effects of sampleorder on accumulation curves), and this rate was signifi-cantly higher in ground-level traps than in upper-leveltraps (ANCOVA, F4,384=562.1, P<0.001). Species rich-ness estimated by rarefaction was also higher in theground-level traps (Fig. 2).

Table 2 shows Morisita-Horn’s measures of similarity(C) among traps. Similarity was greatest among the threesets of traps at ground level (shade, gap and low;C=0.77–0.87). High traps had low similarity to any traps

Table 1 Species richness, abundance and diversity of butterfliessampled in fruit-baited traps (excluding Euthalia/Tanaecia spe-cies). Simpson and Shannon means followed by the same letterare not significantly different at the 5% level (pairwise randomi-sation tests based on 10,000 random samples). Richness=speciesrichness estimate after 65 trap-days using rarefaction (see Fig. 2).Recapture rate (number of recaptures/all capture events) is calcu-lated only for species with ≥10 individuals

Shade Gap Low Medium High2 m 20 m 40 m

Individuals 307 227 299 84 34Capture events 627 391 952 164 48Recapture rate 0.51 0.42 0.69 0.49 0.29Species (total=54) 36 34 35 19 10Richness 35.5 33.6 31.8 16.6 8.9(SE) (0.7) (0.6) (1.6) (1.3) (0.9)Simpson 12.1a 16.8b 11.0a 7.7a 6.2a(95% CI) (±2.1) (±2.5) (±1.6) (±2.3) (±2.4)Shannon-Wiener 2.9a 3.0a 2.8a 2.3b 1.9b

(H′)(variance) (0.004) (0.004) (0.004) (0.013) (0.023)

Fig. 1 Ranked proportional abundance of species in shade (solidbars) and gap (open bars) traps

Fig. 2 Species accumulation curves in low-level traps (open cir-cles gap traps, solid circles shade, solid squares tree platform lowtraps), medium (open squares) and high traps (mottled squares).Data points show estimated species richness (±SE) every 5 daysusing rarefaction

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at ground level (C=0.07 to 0.19), but the greatest similar-ity was with those in gaps (Table 2). Medium-level trapshad intermediate similarity with all other traps (C=0.22to 0.44), but as with the high traps, the greatest similarityto the ground-level traps was with those in gaps.

For those species trapped in all locations (shade, gapand tree platform traps), we investigated the relationshipbetween species’ light habitat preference (gap versusshade) and their height preference (low versus mediumand high tree platform traps). We restricted the analysisto include only species with ≥10 individuals sampled.For each species (n=18), we calculated indices for lightpreference (number of individuals trapped in gaptraps/total number in gap and shade traps; index range0–1 where 0=only caught in shade traps, 1=only caughtin gaps) and height preference (number of individualstrapped in medium and high traps/total number in all treeplatform traps; index range 0–1 where 0=only caught inlow traps, 1=only caught in medium and high traps).There was a significant and positive correlation betweenthese indices (Spearman correlation, rs=0.73, n=18,P<0.001; Fig. 3) showing that species preferring shadetraps were more likely to be trapped in low-level treeplatform traps, and that species preferring gaps weremore likely to be trapped in upper-level traps.

Geographical distribution

Butterflies caught in shade traps had more restrictedgeographical distributions than those caught in gaps(Mann-Whitney, Z=–2.22, P=0.03; median rank inshade traps=16, gap traps=35), and butterflies caught inlow-level traps at the tree platform had more restricteddistributions than those caught in upper-level traps (me-dium and high traps combined; Z=–2.99, P=0.003; me-dian rank in low traps=23, high traps=41). For thosespecies with ≥10 individuals sampled, we also investi-gated the relationship between species’ indices of habi-tat and height preferences (see above) and their geo-graphical distribution. There was a significant positiverelationship between species’ light habitat preferenceand geographical range (Spearman correlation, rs=0.731,n=20, P<0.001) and also between species’ height prefer-ence and geographical range (rs=0.551, n=21, P<0.01)showing that species with more widespread distributionswere more likely to occur in gaps and in canopy traps,and that species with more restricted distributions weremore likely to occur in shade traps and in low-leveltraps.

There were no differences in the proportion of speciesfrom each of the four sub-families trapped in either gapor shade traps (χ2=4.81, 3 df, n=41 cases, P=0.18) butthere were significant differences in the proportioncaught in low and upper-level tree platform traps(χ2=13.32, 3 df, n=44 cases, P=0.004), as well as signifi-cant differences in geographic distribution among sub-families; Satyrinae species had the most restricted distri-butions (median rank=16) and Charaxinae the least (me-dian rank=38; Kruskal-Wallis, χ2=13.02, P=0.005). Thusdifferences in geographical distinctiveness among trapsmay have been affected by phylogeny, and so analyseswere repeated for only one sub-family (Nymphalinae)for which there was a reasonable sample size in all traps(total of 319 individuals of 18 species from 13 genera).This confirmed that butterflies caught in shade traps(median rank=32) had more restricted distributions thanthose in gap traps (median rank=41; Mann-Whitney,Z=–2.13, P=0.03), and that butterflies in low-level traps(median rank=30.5) had more restricted distributionsthan those in upper-level traps (median rank=49.5;Z=–2.31, P=0.02).

Recaptures and movements between traps

Among the traps at ground level, the lowest recapturerate (recapture events/all capture events; Table 1) was inthe gap traps. Recapture rates at the tree platform trapsdeclined with increasing height of traps from the ground.This pattern of recapture rates among traps was similar ifonly species with ≥10 individuals were included. Someindividuals were recaptured moving between traps in dif-ferent habitats, of which the largest number of these re-captures (8%, n=81) were of individuals moving be-tween gap and shade traps. Very few individuals were re-captured moving between tree platform traps at different

Table 2 Morisita-Horn similarity indices

Shade Low Medium High

Gap 0.873 0.771 0.431 0.185Low 0.860 0.405 0.103Medium 0.216 0.439High 0.071

Fig. 3 Correlation between indices of species’ height preferenceand light habitat preference. Indices are based on proportions ofindividuals trapped in different locations for each species with ≥10individuals sampled

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heights; 33 recaptures (3%) were of individuals movingbetween low and medium traps, two recaptures (0.2%)were of individuals moving between medium and hightraps, and two recaptures were of individuals moving be-tween low and high traps. Approximately one-third ofspecies trapped in either gap or shade traps were subse-quently recaptured (n=10 and 13 species, respectively).In both sets of traps, the frequency of recapture amongspecies differed significantly from a Poisson distribution(P<0.0001 in both cases) and variance to mean ratioswere much larger than 1 showing that a small number ofspecies were responsible for the majority of recaptures(Fig. 4). Two species (Neorina lowii and Bassarona dun-ya) were responsible for >45% of all recaptures; bothspecies were more common in shade traps.

Flight morphology

There were significant differences between males and fe-males in the allometric relationship between thorax vol-ume and body length (ANCOVA of thorax volume withsex and sub-family as factors and body length as a co-variate, weighted by sample size; sex by body length in-teraction, F1,58=6.34, P=0.015), and so comparisonsamong traps were carried out separately for each sex. Formales, there was a significant sub-family by trap interac-tion (F3,25=5.63, P=0.004) showing that male Nymphal-inae and Charaxinae in gaps had relatively large thoraxescompared with those in shade traps (ANCOVA of thoraxvolume by trap location, with sub-family (Nymphalinaeor Charaxinae) as a factor, and body length as a covari-ate; F1,13=12.51, P=0.004; Fig. 5). Male Nymphalinaeand Charaxinae in upper-level traps (combining mediumand high traps) also had relatively large thoraxes com-pared with those in low traps (F1,12=8.47, P=0.013).However, this pattern was not observed in other sub-families, or in females.

Butterflies in gaps also had significantly broader thoraxes compared with those caught in shade traps(ANOVA of thorax shape by trap location, with sex andsub-family as factors; trap F1,38=6.18, P=0.017), al-though there were no differences in thorax shape amongtraps at different heights. There were also no significantdifferences among traps in either relative abdomen vol-ume or wing shape. Overall, body morphology differedamong the four sub-families; Satyrinae were the smallest(as measured by body length) and had relatively largeabdomens, Morphinae had relatively large and broadwings, and Charaxinae had relatively large and broadthoraxes.

Discussion

Collection of data

During the study we caught a total of 54 species whichrepresents approximately 70% of the fruit-feeding spe-cies that have been recorded at the study site. This spe-cies richness is similar to that recorded using similarmethods at other sites in Sabah (Schulze and Fiedler1998; Schulze et al., in press). The advantages of usingfruit-baited traps for monitoring butterflies, as opposedto techniques such as walk-and-count transects (follow-ing methods in Pollard 1977) in highly diverse areassuch as southeast Asia were discussed by Walpole andSheldon (1999). Although traps catch only one guild ofbutterflies, they allow more easy access to the canopyand avoid some of the problems of species identificationthat can be encountered using transect techniques. How-ever, it is not known if fruit-traps are equally efficient atattracting and retaining different species. Studies in theNeotropics indicate that although species may vary intheir escape rates, relatively long-term studies such asthis one, which sampled for 1,060 trap days during an

Fig. 4 Proportion of recaptures in shade (solid bars) and gap(open bars) traps. Shade traps, n=13 species where individualswere recaptured, total of 320 recapture events; gap traps, n=10species, total of 164 recapture events)

Fig. 5 Relative thorax volume of male Nymphalinae (circles) andCharaxinae (triangles) butterflies trapped in shade (solid symbols)and gap traps (open symbols)

18-month period, largely avoid these problems (Hugheset al. 1998). Our observations based on 2-hourly checksover a 4-day period (K.C. Hamer and J.K. Hill, unpub-lished work) indicate that <5% of individuals caught intraps during the day escaped before the traps were sam-pled in the afternoon, and that there was no consistentpattern of escape in relation to trap location.

We have some evidence that individuals may re-cognise traps as a source of food and become “trap-hap-py”; one individual of Bassarona dunya was recapturedevery day for 11 days (J. Tangah, unpublished work).This highlights the importance of separating individualdata from recaptures in these type of studies, as also in-dicated by Beck and Schulze (in press). There are no da-ta on the distances over which fruit-traps attract butter-flies or on the size of the area that traps sample. In thisstudy, the low frequency of movements of individualsbetween traps 50–400 m apart, together with the marked-ly different numbers of species and individuals trappedin traps at 2 m and 20 m from the ground indicate thatdistances over which species are attracted to traps maybe relatively short. This agrees with other studies whichalso show distinct butterfly assemblages between traps50–100 m apart (Pinheiro and Ortiz 1992). However, thelarge number of individuals caught in traps suggests thatthe area over which traps sample butterflies may be rela-tively large compared with other sampling techniques(Hamer and Hill 2000). It is likely that species differ intheir attraction to traps, and in this study recapture ratesof species differed significantly from a Poisson distribu-tion. Thus observed differences in relative abundanceamong species may also reflect differences in attractionto traps (Davis and Sutton 1997; Hughes et al. 1998).However, all traps were located in relatively close prox-imity to each other (within an area of <10 ha) in order tominimise beta diversity and so all traps could in princi-ple sample the same local assemblage of butterfly spe-cies. Thus we are confident that differences in relativeabundance of species between habitats reflect differencesin species’ habitat preferences.

Effects of light on butterfly assemblages

There was evidence for a distinctive gap fauna of fruit-feeding nymphalid butterflies; only 60% of species weretrapped in both gap and shade traps and 8 species (18%)were caught only in gaps. Diversity of butterflies in gapswas also higher in terms of species evenness. This sup-ports other studies showing that light is important instructuring tropical forest butterfly assemblages and thatincreased light is associated with increased butterfly di-versity (Sparrow et al. 1994; Pinheiro and Ortiz 1992).Increased butterfly diversity has also been reported in re-sponse to moderate anthropogenic habitat modification(e.g. commercial selective logging, shifting agriculture;Hamer and Hill 2000 and references therein) and habitatfragmentation (Brown and Hutchings 1997; Lovejoy etal. 1986) which opens up the canopy. This is in agree-

ment with the prediction that highest diversity should oc-cur in situations of intermediate disturbance when bothclimax and pioneer species can co-exist (Horn 1975;Connell 1978), although not all studies report a consis-tent response to disturbance (Hamer and Hill 2000).

Measures of diversity give no information on thecomposition of the butterfly fauna and although butterflydiversity was higher in gaps, significantly lower geo-graphical distinctiveness was recorded in butterfly as-semblages in gaps than in shade traps. For example, onlya single individual of the endemic Mycalesis kina wascaught in gaps, compared with 11 individuals trapped inclosed canopy traps. Most studies investigating impactsof anthropogenic habitat modification on butterflies havereported that endemic species and species with restricteddistributions are lost following disturbance (Hill et al.1995; Hamer et al. 1997; Spitzer et al. 1993, 1997; Willott et al. 2000). Results from this study indicate thatthis is most likely to be due to changes in light penetrat-ing the canopy. Many forest butterflies, particularly Satyrinae, are sensitive to changes in moisture availabili-ty and humidity (Hill 1999) and changes in canopy coverand light penetration may impact directly on butterflydistributions through microclimatic effects on adult andlarval survival. Changes in light may also indirectly af-fect butterfly distributions through effects on host plantquality (Blau 1980).

Similarities between gap and canopy assemblages

There was little similarity between butterfly assemblagesof upper-level and ground-level traps, although the great-est similarity with ground-level traps was with traps ingaps. Thus there was some evidence for gaps recordinghigher butterfly diversity than shade traps because gapassemblages were supplemented by canopy fauna. But-terfly diversity declined significantly with height of trapabove the ground (Wood and Gillman 1998; Schulze etal., in press) and this probably reflects the availability ofrotting fruits which may be most likely to fall to theground. However, some canopy species were not record-ed in ground-level traps indicating that some speciesmay feed on fruit rotting in situ, or trapped in the upperbranches. Vertical stratification of butterflies may also be maintained by the location of larval host plants (Beccaloni 1997); for example, many of the Satyrinaefeed as larvae on species of Poaceae which are confinedto ground level (Corbet and Pendlebury 1992; Fiedler1998).

Dispersal rates

Traps in gaps had lower recapture rates and were charac-terised by species with relatively larger and broader tho-raxes. Larger thorax size has been related to higher flightspeed in butterflies (Dempster et al. 1976; Chai and Srygley 1990; Srygley and Chai 1990) indicating that

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butterflies in gaps were capable of faster flight. Taken to-gether, these data suggest that butterflies in gaps weremore mobile and this increased mobility would allowspecies to exploit a more ephemeral and unpredictableresource (Denno et al. 1996). We have assumed that dif-ferences in flight morphology are primarily related todispersal potential in relation to distribution of habitat,although flight has many other functions in butterfliessuch as mate-location and predator-avoidance. Differ-ences in the types of predators and their behaviour in dif-ferent habitats may also select for different flight morph-ologies in butterflies in dense forest versus more openareas (Schulze et al., in press). There are also many dif-ferent aspects to flight (e.g. speed, duration, agility, manoeuvrability) and different adult morphologies areadvantageous for different types of flight (Betts andWootton 1988; Chai and Srygley 1990; Srygley and Chai1990). Differences in vegetation structure in differenthabitats may favour different types of flight; more ma-noeuvrable flight in dense vegetation and faster flight inopen areas. There is some information to suggest thatbroad wings (=lower aspect ratios, Marden 1987) favourslow, agile flight (Betts and Wootton 1988). In this study,Morphinae had relatively broad wings which may favourmore manoeuvrable flight in dense forest where many ofthese species occur (Schulze and Fiedler 1998).

This study has shown that butterfly assemblages aresensitive to changes in canopy openness resulting fromnatural treefalls. Increasing canopy openness results in abutterfly fauna containing fewer species with restricteddistributions and more widespread species. Natural tree-fall gaps comprise <1% of tropical forest areas (Lawtonand Putz 1988), but areas with an open canopy are likelyto increase greatly as a result of anthropogenic modifica-tion. This study indicates that these changes may signifi-cantly reduce the occurrence of species with restricteddistributions.

Acknowledgements We thank all the staff and scientists atDVFC, particularly Glen Reynolds, and also Dr Chey Vun Khen(Forest Research Centre), Dr Maryati Mohamed (Universiti Ma-laysia Sabah). We also thank Yayasan Sabah (Forestry Division),the Danum Valley Management Committee, the State Secretary(Internal Affairs and Research Office), Sabah Chief Minister’s De-partment, and the Economic Planning Unit of the Prime Minister’sDepartment, Kuala Lumpur for permission to conduct research atDanum Valley, Sabah. This study is part of projects DV157 andDV158 of the Danum Valley Rainforest Research and TrainingProgramme and was supported by the British Government’s Dar-win Initiative (DETR). This paper is based on research carriedwhilst the authors were participants in the Royal Society’s SouthEast Asia Rainforest Research Programme (programme publica-tion number A/333).

Appendix 1

Butterfly species were sampled in fruit-baited traps according to trap location

Table A1 Rank ranked geographical distribution (1=endemic,54=most widespread species). Low (2 m), medium (20 m) and high(40 m) refer to height of tree platform traps. First figure in each

column shows the number of individuals caught, followed by thenumber of capture events (if different) in parentheses

Rank Shade Gap Trap location

Low Medium High

SatyrinaeElymnias panthera Fabric 17 – 1 – – –Melanitis leda L. 54 6 6 17 (23) 17 (20) 7 (10)Neorina lowii Doub. 17 65 (110) 27 (28) 51 (152) 1 –Mycalesis anapita Moore 6 17 (9) 18 (4) 4 (1) 1 –M. patiana Eliot 3 19 (28) 11 (12) 4 1 –M. kina Staud. 1 6 (9) 1 5 (8) – –M. dohertyi Elwes 6 3 – 1 – –M. horsfieldi Moore 23 5 3 3 – –M. maianeas Hewit. 6 15 (18) 3 4 (3) – –M. oroatis Hewit. 17 – – 2 – –M. orseis Hewit. 26 28 (41) 23 (27) 16 (20) – –M. janardana Moore 26 1 1 1 – –Erites elegans Butler 6 – 1 1 – –Ragadia makuta Horsfield 17 13 (14) 7 18 – –Coelites epiminthia West. 26 – 1 – – –

MorphinaeFaunis gracilis Butler 6 1 – – – –F. canens Hubner 33 – – 1 – –F. kirata de Niceville 6 1 – – – –F. stomphax West. 6 1 – 2 (3) – –Xanthotaenia busiris West. 17 – – 1 – –Amathusia phiddippus L. 30 1 6 1 (2) 5 (6) 2

301

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