6
J. Zool., Lond. (2004) 263, 135–140 C 2004 The Zoological Society of London Printed in the United Kingdom DOI:10.1017/S0952836904004959 What causes the vulnerability of endemic animals? A case study from Sri Lanka Mayuri R. Wijesinghe* and M. de L. BrookeDepartment of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K. (Accepted 10 November 2003) Abstract Around the world, endemic species with restricted ranges seem to be at particular risk of extinction. When range size is controlled, lowland continental species may be especially at risk, more so than island or montane species. Our study aimed to investigate reasons behind the high vulnerability of endemic species. In Sri Lanka, large- scale national surveys and intensive localized fieldwork established that endemic plant and animal species are mostly associated with undisturbed rainforest habitats. On the other hand, non-endemic species used both forest and non-forest habitats almost equally, suggesting they are less likely to suffer from deleterious edge effects. To understand the different distribution of endemic and non-endemic species, our study focused on rats. Compared to the widespread species, the endemic rat species had a larger home range and fed on fewer species of forest fruit, possibly indicating greater specialization. The abundance of the endemic species was also negatively correlated with the abundance of the non-endemic species, to which it was behaviourally subordinate. Greater specialization and competitive inferiority could both contribute to the vulnerability of endemic species. Key words: Rattus, Srilankamys, competition, radio-tracking, diet specialization, endemism INTRODUCTION As the threat of extinction hangs over a significant pro- portion of the earth’s biota, endemic species with restricted range are most at risk (Bibby, Collar et al., 1992). When range size is controlled, lowland bird species are at greater risk than montane or island taxa (Manne, Brooks & Pimm, 1999). But it is not altogether clear, at a proximate level, why species with modest ranges should be so vulnerable. Although a modest range is likely to be associated with a moderate overall population size, and consequent vulnerability to stochastic effects on population size, this is not obviously a sufficient explanation for the greater vulnerability of endemics. Illuminating the matter could assist the conservation of endemic species. Endemic species are characteristically associated with undisturbed habitats (Myers et al., 2000). Although such an association could itself contribute to the vulnerability of endemics, since habitat disturbance would potentially lead to population decline, the observation does not Present address: Department of Zoology, University of Colombo, Colombo 03, Sri Lanka. All correspondence to: M. de L. Brooke, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K. E-mail: [email protected] itself explain the underlying cause(s). On the other hand, widespread or non-endemic species may be found in a range of habitats, including those anthropogenically altered, and this is part of the reason why they are widespread. Basing our study in Sri Lanka, an island with a high level of endemism and rich in biodiversity endemics (Gunatilleke & Gunatilleke, 1981; Myers et al., 2000), we first assessed whether this general statement – endemic species are largely restricted to undisturbed habitats in contrast to non-endemics in a variety of habitats – held in Sri Lanka. From our studies in the wet south-west of the island, where there is a high concentration of endemic species and biodiversity is at its richest, it emerged that endemic birds and mammals indeed tended to occur mostly within little- disturbed rainforest, while non-endemics tended to be as abundant in forest as in surrounding disturbed habitats. Our study proceeded to address two non-exclusive hypotheses for this observation: (1) that endemics are more specialized, needing resources available only in undisturbed habitats; (2) that endemics are competitively excluded from disturbed or fragmented habitats by non-endemic species. Both greater specialization and competitive exclusion could act to confine endemic species to undisturbed habitats and place them at greater risk of extinction when such habitats are destroyed or fragmented.

What causes the vulnerability of endemic animals? A case study from Sri Lanka

Embed Size (px)

Citation preview

Page 1: What causes the vulnerability of endemic animals? A case study from Sri Lanka

J. Zool., Lond. (2004) 263, 135–140 C© 2004 The Zoological Society of London Printed in the United Kingdom DOI:10.1017/S0952836904004959

What causes the vulnerability of endemic animals? A case studyfrom Sri Lanka

Mayuri R. Wijesinghe* and M. de L. Brooke†Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K.

(Accepted 10 November 2003)

AbstractAround the world, endemic species with restricted ranges seem to be at particular risk of extinction. When rangesize is controlled, lowland continental species may be especially at risk, more so than island or montane species.Our study aimed to investigate reasons behind the high vulnerability of endemic species. In Sri Lanka, large-scale national surveys and intensive localized fieldwork established that endemic plant and animal species aremostly associated with undisturbed rainforest habitats. On the other hand, non-endemic species used both forestand non-forest habitats almost equally, suggesting they are less likely to suffer from deleterious edge effects. Tounderstand the different distribution of endemic and non-endemic species, our study focused on rats. Compared tothe widespread species, the endemic rat species had a larger home range and fed on fewer species of forest fruit,possibly indicating greater specialization. The abundance of the endemic species was also negatively correlatedwith the abundance of the non-endemic species, to which it was behaviourally subordinate. Greater specializationand competitive inferiority could both contribute to the vulnerability of endemic species.

Key words: Rattus, Srilankamys, competition, radio-tracking, diet specialization, endemism

INTRODUCTION

As the threat of extinction hangs over a significant pro-portion of the earth’s biota, endemic species with restrictedrange are most at risk (Bibby, Collar et al., 1992). Whenrange size is controlled, lowland bird species are at greaterrisk than montane or island taxa (Manne, Brooks & Pimm,1999). But it is not altogether clear, at a proximate level,why species with modest ranges should be so vulnerable.Although a modest range is likely to be associatedwith a moderate overall population size, and consequentvulnerability to stochastic effects on population size, thisis not obviously a sufficient explanation for the greatervulnerability of endemics. Illuminating the matter couldassist the conservation of endemic species.

Endemic species are characteristically associated withundisturbed habitats (Myers et al., 2000). Although suchan association could itself contribute to the vulnerabilityof endemics, since habitat disturbance would potentiallylead to population decline, the observation does not

∗Present address: Department of Zoology, University of Colombo, Colombo03, Sri Lanka.†All correspondence to: M. de L. Brooke, Department of Zoology, Universityof Cambridge, Downing Street, Cambridge CB2 3EJ, U.K.E-mail: [email protected]

itself explain the underlying cause(s). On the other hand,widespread or non-endemic species may be found ina range of habitats, including those anthropogenicallyaltered, and this is part of the reason why they arewidespread. Basing our study in Sri Lanka, an islandwith a high level of endemism and rich in biodiversityendemics (Gunatilleke & Gunatilleke, 1981; Myers et al.,2000), we first assessed whether this general statement –endemic species are largely restricted to undisturbedhabitats in contrast to non-endemics in a variety ofhabitats – held in Sri Lanka.

From our studies in the wet south-west of the island,where there is a high concentration of endemic species andbiodiversity is at its richest, it emerged that endemic birdsand mammals indeed tended to occur mostly within little-disturbed rainforest, while non-endemics tended to be asabundant in forest as in surrounding disturbed habitats.Our study proceeded to address two non-exclusivehypotheses for this observation: (1) that endemics aremore specialized, needing resources available only inundisturbed habitats; (2) that endemics are competitivelyexcluded from disturbed or fragmented habitats bynon-endemic species. Both greater specialization andcompetitive exclusion could act to confine endemicspecies to undisturbed habitats and place them at greaterrisk of extinction when such habitats are destroyed orfragmented.

Page 2: What causes the vulnerability of endemic animals? A case study from Sri Lanka

136 M. R. WIJESINGHE AND M. DE L. BROOKE

STUDY AREA AND METHODS

In our study, an endemic taxon is classified as one whoseglobal geographic range does not extend beyond the islandof Sri Lanka (Anderson, 1994). To test for countrywideassociations between endemic taxa from various groups,we draw on data from 189 forest patches surveyed acrossSri Lanka during the 1991–1996 National ConservationReview (IUCN/WCMC, 1997). This was a rapid assess-ment survey of the number of woody plant, mollusc,butterfly, amphibian, reptile, bird and mammal speciesin forest patches of 200 ha or more in extent. While thearea of each patch was known, the shape and perimeterlength, both possible influences on species composition(Laurance, 1994; Williams & Pearson, 1997), were notknown. Annual rainfall, an important determinant ofspecies richness in Sri Lanka, was recorded at each site.

Our main study area was Sinharaja (11 300 ha), whichlies in Sri Lanka’s wet zone and is the largest tract ofintact rainforest on the island. There, a coarse investigationof whether non-endemic animals were more catholic intheir habitat use than endemics was carried out. Twentyto 24 plots of c. 0.25 ha were established in each of4 habitats (primary forest, selectively logged primaryforest, plantation areas, and abandoned agricultural plotsthat had been cleared, cultivated, and then abandonedallowing reversion to secondary vegetation) within oradjacent to Sinharaja. Small mammals were then trappedin each of the 84 plots. Each plot was trapped using 48–50 traps for 1 period of 4 consecutive nights in May–August 1998 or 1999. The plots were at least 500 m fromeach other to minimize the possibility of interchange.

In the same plots as used for mammal trapping, thenumber of birds registered in 2 recording periods of30 min in either 1999 or 2000 was noted. This simplemethodology does not allow comparison between speciesbut, assuming that a species does not differ in detectabilitybetween habitats, should allow comparison of the abund-ance of a species in different habitats (Bibby, Burgess &Hill, 1992).

To investigate differences in fine-grained habitat usebetween endemic and non-endemic taxa, we radio-tracked,in 6 different forest sites within Sinharaja, an adult femaleof each of 3 rat taxa, Srilankamys ohiensis (endemicgenus), and 2 endemic subspecies of the non-endemicspecies Rattus rattus, R. r. kelaarti (confined to wet forestsof Sri Lanka) and R. r. kandianus (widespread acrossthe island). There were no significant mass differencesbetween the 3 taxa. Each female was tracked for 3–4 weeksuntil at least 100 night-time fixes had been gathered on itsmovements. This tracking was considered sufficient sinceprior trials (not reported in detail here) on rats of all 3 taxahad shown a home-range size asymptote was reached afterc. 75 fixes per animal were obtained over c. 3 weeks.

Any differences in home-range size that emerged fromradio-tracking might partly be the result of differences indiet breadth: the greater the breadth, the smaller the homerange. This was explored further in cafeteria experimentsusing fruits from 25 tree species, 24 from the forest, and1 from the adjoining area. Because of the difficulty of

simultaneously obtaining all 25 fruit types tested, 10 fruitspecies were presented at a time (2 fruits of each type)to a rat and whether the fruits were eaten, either fully orpartially, or shunned was recorded. Each fruit type wastested on 15–20 rats of both sexes from each taxon, anda given fruit type on an equal number of animals of eachtaxon.

Captive rats were also tested for their ability to maintainweight over 3 days on a diet of fruit, presented in excess1 species at a time, with water ad libitum. Five individualsfrom each taxon were tested on each fruit type.

While the above methods bear on the possibly greaterdietary specialization of endemics, other methods wereused to test the possibility of competitive exclusion bynon-endemics. First, rats were trapped in 8 forest patchesoutside Sinharaja ranging in size from 400 to 6000 ha(300 trap-nights per patch). Second, the abundance ofthe rat taxa within the 44 trapped forest plots withinSinharaja (see above) was compared. Within those plots,a suite of habitat variables that might influence rat density(Wijesinghe, 2001) was also measured. Third, interspeciesdyadic encounters were staged in the laboratory, allowing2 rats from different taxa to compete for a piece of lightlycharred coconut, food that is readily eaten by the testedspecies. The winner in each case was the individual thatfirst procured the given food item.

RESULTS

Analysis of data from the 189 forest patches establishedthat species richness of endemic and non-endemic taxawas positively significantly correlated with patch area(P < 0.01) for all seven groups (see Methods). Speciesrichness was also significantly correlated with rainfall(P < 0.01), but here the sign of the correlation varied.Although this correlation was always positive for thefive endemic groups (woody plants, molluscs, amphibia,reptiles, birds), it varied for the non-endemics. It waspositive for woody plants, amphibia and reptiles, butnegative for molluscs, butterflies, birds and mammals(Wijesinghe, 2001). To explore the impact of woodyplant species richness on faunal richness, it was evidentlynecessary to control for rainfall and area. When this wasdone, the number of endemic animal species in a forestpatch in four groups (molluscs, amphibians, reptiles,birds) was found to be more closely correlated with thenumber of endemic woody plants in the forest patch thanwith the number of non-endemic woody plants, althoughthe difference was significant only for molluscs (Table 1).On the other hand, the situation was reversed for non-endemic animal taxa which were significantly moreclosely associated with non-endemic woody plants thanwith endemic woody plants (butterflies, reptiles, birds,mammals) or showed no significant difference (molluscs,amphibians). Thus, countrywide, there tended to be apositive association between endemic plants and endemicanimals.

Such an association also emerged when the focus wason mammals and birds within Sinharaja and its immediate

Page 3: What causes the vulnerability of endemic animals? A case study from Sri Lanka

Vulnerability of endemic animals 137

Table 1. Residual species richness of endemic and non-endemic faunal taxa regressed against the residual species richness of endemicand non-endemic woody plants in each of 189 Sri Lankan forest patches, after stripping the effects of area and rainfall. ∗, P < 0.05; ∗∗,P < 0.01; ∗∗∗, P < 0.001; NS, not significant

Endemic woody plants Non-endemic woody plants

R2 Slope P R2 Slope P t a

MolluscsEndemic 0.177 0.49 ∗∗∗ 0.017 0.31 ∗ 3.07∗

Non-endemic 0.000 0.0 NS 0.018 0.18 ∗ 1.30

ButterfliesNon-endemic 0.048 − 0.30 ∗∗ 0.231 1.15 ∗∗∗ 2.91∗

AmphibiansEndemic 0.072 0.23 ∗∗∗ 0.007 0.16 NS 1.84Non-endemic 0.025 0.14 ∗ 0.008 − 0.17 NS 0.68

ReptilesEndemic 0.089 0.28 ∗∗∗ 0.054 0.40 ∗∗ 0.69Non-endemic 0.027 0.18 ∗ 0.135 0.69 ∗∗∗ 2.12∗

BirdsEndemic 0.041 0.16 ∗∗ 0.009 0.16 NS 1.06Non-endemic 0.020 − 0.12 ∗ 0.273 0.75 ∗∗∗ 4.23∗

MammalsNon-endemic 0.007 −0.06 NS 0.140 0.43 ∗∗∗ 2.98∗

a t-values test significance of differences between the contributions of endemic and non-endemic plants to species richness of the givenfaunal group. All variables were log transformed prior to analysis.

environs. After 15 968 trap nights in May–August 1998and 1999, 625 different individual small mammals werecaught, belonging to 12 taxa, five of which are endemicto Sri Lanka. Overall, 246 endemics were caught inforest plots, 30 in non-forest plots, namely plantationareas or abandoned agricultural plots. The correspondingtotals for non-endemics were 139 and 210, respectively.Seven of the 12 species showed significant differences(ANOVA) in abundance between habitats, as follows. Fourendemic and one non-endemic taxa were more abundant inforest habitats, while two non-endemic species were moreabundant in the non-forest habitats. As a result of thesedifferences, forest habitats were occupied by roughly equalnumbers of endemic and non-endemic mammal taxa,while non-endemics were more numerous than endemicsin the disturbed habitats (Fig. 1a).

In the same plots, the number of birds registered in two30-min recording periods was noted. From the 66 speciesrecorded, further analysis was only undertaken of the 53species where > 10 individuals were registered. Of the20 endemic species, 19 were more abundant (ANOVA,P < 0.05) in forest habitats, and the final species showedno significant difference in abundance between habitats.Of the 33 non-endemics, 10 were significantly moreabundant in forest habitats, seven more abundant in non-forest, and 16 showed no difference. As was true ofmammals, forest habitats were occupied by roughly equalnumbers of endemic and non-endemic bird species whilemore non-endemic than endemic species were recorded inthe disturbed habitats (Fig. 1b).

That the association between endemic animals andforest habitats might be the result of greater specializationof the endemics was first explored by comparing homeranges of radio-tracked females. Using a minimum convex

polygon method, mean home ranges (± SE) were 2.25 ±0.37 ha for S. ohiensis, 1.13 ± 0.32 ha for R. r. kelaartiand 0.80 ± 0.17 ha for R. r. kandianus (two-wayANOVA, between-species F2,10 = 25.3, P < 0.001). Themore restricted a taxon, the larger its home range and,possibly therefore by implication, the sparser the resourcesneeded for maintenance.

This possibility was reinforced by the results of thecafeteria experiment. While the endemic Srilankamysate 17 fruit types and shunned eight, both subspeciesof R. rattus ate 20 and shunned five (χ2 = 1.32, 2 d.f.,NS). Four fruit species showed significant differences inconsumption patterns between rat taxa (χ2 tests, P < 0.02,on Doona congestiflora, Syzygium neesianum, Gomphiaserrata and Melastoma malabathricum), in all casesbecause R. rattus were more likely to consume them.

The widespread R. r. kandianus could maintain weighton 15 (of 25) fruits, R. r. kelaarti on 13 and Srilankamyson nine.

Although these results suggest that Srilankamysrequires a larger home range because it feeds on anarrower range of items than R. rattus, the possibilitythat Srilankamys is excluded from non-forest habitats, notonly by a scarcity of suitable food but also by competitiveinteractions with R. rattus, remains. This was investigatedin the three ways described in Methods.

First, in the eight forest patches, abundance(individuals/100 trap nights) of R. r. kandianus was 17.2− 0.00167 area (ha) − 0.00935 elevation (m) − 0.0006annual rainfall (mm) (r2 = 0.835, P < 0.05). ThusR. r. kandianus abundance was negatively associated withpatch area. There was no association between Srilankamysabundance and the three variables (r2 = 0.143, P > 0.05).Rattus r. kelaarti was not caught during these surveys.

Page 4: What causes the vulnerability of endemic animals? A case study from Sri Lanka

138 M. R. WIJESINGHE AND M. DE L. BROOKE

6

5

4

3

2

1

0

(a)

Unlogged Logged Abandoned Plantation

Habitat type

35

30

25

20

15

10

5

0

Num

ber

of s

peci

es

(b)

Fig. 1. (a) Number of endemic (n = 5) and non-endemic(n = 7) small mammal species occupying each of four habitatswithin (unlogged or selectively logged) or around (abandoned orplantation) Sinharaja forest; (b) number of endemic (n = 21) andnon-endemic (n = 45) bird species occupying each of the same fourhabitats within or around Sinharaja forest. Solid bars, endemic taxa;open bars, non-endemics.

Second, trapping within Sinharaja in 44 forest plotsrevealed a strong negative correlation between the abund-ance of Srilankamys and R. r. kandianus (r =− 0.65, P< 0.001), but not between Srilankamys and R. r. kelaarti(r = 0.11, P > 0.05) or the two R. rattus subspecies(r =− 0.22, P > 0.05). Further, logistic regression of asuite of habitat variables and rat abundance showed that,for both Srilankamys and R. r. kandianus, the mostimportant variable predicting the abundance of one wasthe abundance of the other (Table 2), suggesting comp-etitive interactions.

Third, the staged dyadic encounters showed that R. r.kandianus was dominant over the other two taxa, while

Table 2. Ideal models of the abundance of Srilankamys ohiensis,Rattus rattus kelaarti and R. r . kandianus generated by stepwiselogistic regression analysis of data from 44 forest plots in Sinharaja,Sri Lanka

β SE t P

S. ohiensisConstant 2.25 0.936 2.70 0.02Litter depth 1.18 0.507 2.34 0.05Decaying logs present − 0.789 0.418 1.89 0.10R. r. kandianus abundance − 0.468 0.106 4.42 0.0001

Variation explained by ideal model 51.1% F3,40 = 17.6, P < 0.001R. r. kelaartiConstant 3.81 1.19 3.21 0.005Litter cover (%) − 0.044 0.020 2.20 0.05R. r. kandianus abundance − 0.181 0.84 2.155 0.05

Variation explained by ideal model 16.3% F2,41 = 4.88, P < 0.05R. r. kandianusConstant 6.64 1.43 4.63 0.0001Rock cover (%) 0.091 0.030 3.03 0.005Litter cover (%) − 0.089 0.028 3.18 0.005Height of largest tree in plot 0.061 0.036 1.69 0.10S. ohiensis abundance − 0.666 0.114 5.84 0.0001R. r. kelaarti abundance − 0.411 0.192 2.14 0.05

Variation explained by ideal model 64.9% F5,38 = 20.3, P < 0.001

Srilankamys was dominant over R. r. kelaarti. A significantmajority of interactions was won by R. r. kandianuscompeting with Srilankamys (χ2 = 12.5, 1 d.f., P < 0.001)and with R. r. kelaarti (χ2 = 30.4, 1 d.f., P < 0.001).Likewise Srilankamys was significantly more likely to winthan to lose when competing with R. r. kelaarti (χ2 = 30.7,1 d.f., P < 0.001). Contest outcomes were not affectedby the weights of the participants. Wijesinghe (2001)provides further details.

DISCUSSION

The results of the countrywide analysis (Table 1) indicatean association between endemic animals and forestpatches rich in endemic plants, an association whichcould have arisen in several ways. It could have arisenbecause of similar historical factors promoting endemicityin plants and animals, for example isolation of biotawhen the land bridge connecting Sri Lanka to the Indiansubcontinent was severed, or when the south-central partof Sri Lanka was uplifted and differentiated from thelowlands to the north and east (Wadia, 1941; Jacob, 1949).In such a case the result would not necessarily implyany ongoing ecological connection between endemictaxa. However, the result could also reflect modernecological interdependence between endemic plants andanimals. Such interdependence would contribute to thevulnerability of endemics, the focus of this study.

While the endemic mammals and birds of the Sinharajaarea were largely confined to forest habitats, the non-endemics were roughly equally numerous in forested anddisturbed habitats, and this was true both for species

Page 5: What causes the vulnerability of endemic animals? A case study from Sri Lanka

Vulnerability of endemic animals 139

(Fig. 1) and individuals per species. This suggests thatthe non-endemics are less vulnerable to the edge effectsthat will impact increasingly adversely on the forest-dwelling endemics as forest habitats become fragmented(Laurance, 1994; Stevens & Husband, 1998; Thiollay,1999).

Two potential explanations for the scarcity of endemicsin disturbed habitats are either that they required some re-sources available in forest but scarcer in disturbed habitats,and/or they were excluded from the latter by competitiveinteractions with non-endemics (McKinney, 1997). Insupport of the former, the endemic rat Srilankamys,although morphologically similar, was found to have alarger home range than two subspecies of the widespreadR. rattus. This suggests that the resources required bySrilankamys were sparser. In accord with this suggestion,Srilankamys shunned more species and could not maintainweight on more species of forest fruit than was true ofeither subspecies of R. rattus. However, analysis of thosefruits eaten by the rats from the 25 species offered (data notpresented) did not support the possibility that Srilankamyswas more (or less) dependent on the fruits of endemicplant species than was R. rattus. But the 25 species thatwere presented were under half of the species potentiallyavailable in Sinharaja (Gunatilleke & Gunatilleke, 1985).

In support of competitive exclusion of one species bythe other, a strong negative correlation was found betweenthe presence of Srilankamys and R. r. kandianus. Couplethis with the behavioural dominance of R. r. kandianus instaged encounters and the evidence, from the survey ofeight forest patches, that the latter is more numerous insmaller patches, and it would be expected that the endemicSrilankamys would be scarce or absent in smaller forestpatches.

These findings have relevance to ideas about a ‘taxoncycle’, primarily developed for islands smaller than SriLanka (Wilson, 1961; Ricklefs & Cox, 1972). Under thecycle, it was envisaged that successful colonist specieswould occupy a wide range of habitats, allowing rapidpopulation expansion. In time, the biotic environment(e.g. predators, food sources) of the island would adjust tothe colonist species, reducing its population and forcingit to become more specialized. Still later, the increasingspecialization and the arrival of other colonizing speciescould lead to extinction, hence a cycle. But the idea couldalso be relevant to larger islands, such as Sri Lanka, andindeed to habitat islands within continental areas, althoughdetecting any cycle in the latter would be problematical.

Some authors (e.g. Losos, 1992; Roughgarden, 1992)have investigated size differences between colonizingand established species, but there was no indication thatthis was a critical factor in the interactions between therats in our study. Indeed the general vulnerability ofendemics points to their being disadvantaged on manyfronts.

In summary, in Sri Lanka where the endemic animalsare significantly associated with wet zone primary forest,our work shows that rats of the endemic genus Srilankamysuse a larger home range than other rats. This seems partlya consequence of a more specialized diet. These factors

render the species susceptible to forest fragmentation,a predicament compounded because it is behaviourallysubordinate to the invasive R. r. kandianus, which is morenumerous in smaller forest fragments. If these results canbe generalized to other species and systems, they helpexplain the particular vulnerability of endemic taxa toanthropogenic habitat change.

Acknowledgements

We are very grateful to the Association of CommonwealthUniversities and the Hans Gadow Memorial Trust,University of Cambridge, for supporting this work.Andrew Balmford, Tim Coulson and Oliver Kruger andtwo anonymous referees helpfully commented on draftsof the paper.

REFERENCES

Anderson, S. (1994). Area and endemism. Q. Rev. Biol. 69: 451–471.

Bibby, C. J., Burgess, N. D. & Hill, D. A. (1992). Bird CensusTechniques. London: Academic Press.

Bibby, C. J., Collar, N. J., Crosby, M. J., Heath, M. F., Imboden,Ch., Johnson, T. H., Long, A. J., Stattersfield, A. J. & Thirgood,S. J. (1992). Putting biodiversity on the map: priority areas forglobal conservation. Cambridge: International Council for BirdPreservation.

Gunatilleke, C. V. S. & Gunatilleke, I. U. A. N. (1981). The floristiccomposition of Sinharaja: a rainforest in Sri Lanka with specialreference to endemics and dipterocarps. Malays. For. 44: 386–396.

Gunatilleke, C. V. S. & Gunatilleke, I. U. A. N. (1985).Phytosociology of Sinharaja – a contribution to rain-forestconservation in Sri Lanka. Biol. Conserv. 31: 21–40.

IUCN/WCMC. (1997). Designing an optimum protected areasystem for Sri Lanka’s natural forest. Colombo and Cambridge:The World Conservation Union and World ConservationMonitoring Centre.

Jacob, K. (1949). Land connections between Ceylon and India.Proc. Natl Inst. Sci. 16: 341–343.

Laurance, W. F. (1994). Rainforest fragmentation and the structureof small mammal communities in tropical Queensland. Biol.Conserv. 69: 23–32.

Losos, J. B. (1992). A critical comparison of the taxon-cycleand character-displacement models for size evolution of Anolislizards in the Lesser Antilles. Copeia 1992: 279–288.

Manne, L. L., Brooks, T. M. & Pimm, S. L. (1999). Relative risk ofextinction of passerine birds on continents and islands. Nature(Lond.) 399: 258–261.

McKinney, M. L. (1997). Extinction vulnerability and selectivity:combining ecological and paleontological views. Annu. Rev.Ecol. Syst. 28: 495–516.

Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca,G. A. B. & Kent, J. (2000). Biodiversity hotspots for conservationpriorities. Nature (Lond.) 403: 853–858.

Ricklefs, R. E. & Cox, G. W. (1972). Taxon cycles in the WestIndian avifauna. Am. Nat. 106: 195–219.

Roughgarden, J. (1992). Comments on the paper by Losos: characterdisplacement versus taxon loop. Copeia 1992: 288–295.

Stevens, S. M. & Husband, T. P. (1998). The influence of edgeon small mammals: evidence from Brazilian Atlantic forestfragments. Biol. Conserv. 85: 1–8.

Page 6: What causes the vulnerability of endemic animals? A case study from Sri Lanka

140 M. R. WIJESINGHE AND M. DE L. BROOKE

Thiollay, J. M. (1999). Responses of an avian community torainforest degradation. Biodivers. Conserv. 8: 513–534.

Wadia, D. N. (1941). The making of Ceylon. Spolia Zeylan. 23: 1–7.Wijesinghe, M. R. (2001). Habitat selection of endemic and non-

endemic vertebrates in Sinharaja, a rainforest in Sri Lanka. PhDthesis, University of Cambridge.

Williams, S. E. & Pearson, R. G. (1997). Historical rainforestcontractions, localized extinctions and patterns of vertebrateendemism in the rainforests of Australia’s wet tropics. Proc. R.Soc. Lond. B Biol. Sci. 264: 709–716.

Wilson, E. O. (1961). The nature of taxon cycle in the Melanesianant fauna. Am. Nat. 95: 169–193.