Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar

Biological Conservation 96 (2000) 31±43

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In¯uence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar Denis Vallan * Zoological Institute, University of Bern, Baltzerstrasse 3, 3012 Bern, Switzerland Received 26 March 1999; received in revised form 19 January 2000; accepted 26 January 2000

Abstract In Ambohitantely the rainforest is divided distinctly by pseudosteppe into more than 500 fragments. The amphibian faunas of seven such fragments varying in size from 0.16 to 1250 ha were examined. Twenty-eight amphibian species of two families (Ranidae and Microhylidae) were recorded in the rainforest fragments. The species numbers in the fragments were positively correlated with fragment area and form nested subsets. Composition and individual frequency in small fragments di€ered from that of the control site (1250 ha). The relative individual density (individuals found each searching hour) was negatively correlated with the fragment size. This is probably due to the fact that the density of streams and brooks was higher in small fragments, which also explains why smaller fragments contained a larger proportion of brook-dwelling amphibian species than larger fragments. Species that live far from water and show a reproduction strategy independent of running waters or ponds, such as certain microhylids, were only present in fragments of 30 ha or more. The more common species in the control site were also found in the majority of fragments. A rainforest remnant of 1250 ha seems to be large enough to contain a large part of the original amphibian fauna, provided that there are suitable microhabitats. Compared to other taxa, amphibians generally seem to react less sensitively to fragmentation. Due to the sensitivity to microclimate changes microhylids and certain species of the subfamily of Mantellinae represent good bioindicators. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Habitat loss; Rain forest; Amphibian community; Madagascar; Nested subset

1. Introduction Shortly after the colonisation of Madagascar by humans, about 2000 years ago, the deforestation of the natural forests began. By 1600 AD many forests, especially in the highlands, were already destroyed (Battistini and VeÂrin, 1972; Gade, 1996). Green and Sussman (1990) have documented a rapid decline in rainforest during the past decades. The deforestation of a rainforest is nearly always accompanied by fragmentation. If management guidelines for a cohabitation of humans and the rest of nature are to be established it is of the utmost importance to know the requirements of the animal species concerned in order to be able to make statements on minimal areas and structures of their habitat. Publications on this subject deal mainly with birds (e.g. Galli et al., 1976; Blake and Karr, 1984; Dowsett-Lemaire and Dowsett, 1984; Bierregaard and Lovejoy, 1989; Newmark, 1991; Keyser et al., 1998), * Tel.: +49-31-631-45-25; fax: +41-31-631-48-88. E-mail address: [email protected] .

and mammals (e.g. Laurance, 1990; Laurance, 1994; Goodman and Rakotondravony, in press) but only a few deal with reptiles or amphibians (Marsh and Pearman, 1997; Tocher et al., 1997) The abundance of publications on the world wide decline in amphibian diversity and density (e.g. Barringa, 1990; Blaustein and Wake, 1990; Johnson, 1992; Richards et al., 1993; Blaustein, 1994; Delis et al., 1996; Donnelly, 1998) is evidence of amphibians' sensitivity to environmental change. Even if the causal connections may not always be clear (Pechman and Wilbur, 1994), it must be assumed that amphibians are extremely sensitively to habitat perturbations, particularly owing to the fact that during their ontogenesis they are exposed to various environmental factors. Ambohitantely is a nature reserve situated in Madagascar's highlands and divided into several hundred forest fragments (Langrand and WilmeÂ, 1997) which are ideal for research on the in¯uence of fragmentation on various types of organisms. Ambohitantely has been the site for research studies on the consequences of anthropogenic activities on rainforest fauna (birds: Langrand, 1995;

0006-3207/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(00)00041-0

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D. Vallan / Biological Conservation 96 (2000) 31±43

Langrand and WilmeÂ, 1997; Wilme et al., in press; mammals: Stephenson et al., 1994; Goodman and Rakotondravony, in press). The aim of the present study was to determine the e€ects of rainforest fragmentation (size of habitat) on the diversity of amphibians. The main question to be answered was if and how the amphibian diversity and density changes with decreasing fragment size. If such changes occur, are they changes associated with deterministic or stochastic processes? Which taxa or guilds react most sensitively to the reduction of habitat size? Can any statements be made on the minimal size of a habitat necessary to preserve a large part of the original amphibian diversity? 2. Study area and methods 2.1. Study area The research study took place in the ``ReÂserve SpeÂciale'' (RS) d'Ambohitantely, a nature reserve in central highland Madagascar, 135 km north-east of the capital Antananarivo. This reserve lies between 1300 and 1650 m a.s.l. and covers an area of 5600 ha (Nicoll and Langrand, 1989). The RS contains some of the very last remains of central high plateau rainforest, which Koechlin (1972) described as ``high-altitude lichen forest''. Fifty per cent of the area is made up of natural forests, 35% are anthropogenic pseudosteppes (see Koechlin et al. 1997 for the de®nition of pseudosteppe) and 15% are exotic tree plantations (Langrand and WilmeÂ, 1997). On the basis of soil analysis, Riguier (1951) suspects that Ambohitantely was once primarily covered with forest, yet more recent studies using pollen analysis (e.g. MacPhee et al., 1985; Burney, 1987) on several sites in the central highlands have shown that the vegetation around 5000 BC consisted of a mosaic of forest, bush and natural savannah. In 1897 the largest contiguous rainforest block at Ambohitantely was estimated to have a length of 20 km (Langrand and WilmeÂ, 1997). In 1988 Seguier-Guis estimated the same forest's length to be merely 8 km. According to Bastian (1964) the forested landscape made up 3000 ha in 1964, 2000 of which were one contiguous block of forest. The RS d'Ambohitantely now consists of hundreds of islands of forest, their sizes ranging from 0.16 to 1250 ha making up a total of 2737 ha, about half the total reserve area (Langrand and WilmeÂ, 1997) (Fig. 1). About 78% of the fragments are <3 ha (Langrand and WilmeÂ, 1997). In most cases the ecotone between forest and surrounding pseudosteppe is very sharp. A large number of the fragments in Ambohitantely persist near brooks or streams in the valleys. Nearly all the original vegetation, which was very sensitive to ®re and drought, has been burned down to create pasture for cattle (Koechlin et al.

1997). Rajoelison (1990) and Razakanirina (1993) distinguish four di€erent types of forest: (1) Riparian forest: this three-layer forest type is found at the bottoms of forested valleys. The canopy is about 20 m high. The undergrowth shows relatively sparse vegetation. Emergent trees reach up to 30 m. The litter and soil layers are thicker than in the other forest types. Of the four forest types, riparian forest displays the highest tree species diversity. (2) Slope forest: the average height of the canopy of this three-layered forest is about 16 m. A characteristic middle layer is often rich in bamboos. (3) Plateau forest: the canopy of this two-layer forest reaches 10±12 m. The microclimate is drier with sclerophyll and microphyll plants more common than in the slope forest and riparian forest. (4) Ridge forest: Dense type of forest consisting of short, thin trees. The canopy height is 5±10 m. Sclerophylly and microphylly is very distinct. 2.2. Climate The data on climate of the years 1981±1996 are taken from the forest station of FOFIFA-DRFP in Manankazo (1580 m a.s.l., 7 km away from the edge of RS d'Ambohitantely). The area has a high-altitude tropical climate with a warm, wet season and a cool, dry season (Donque, 1972). An annual average precipitation of 1885 mm is distributed over 184 days with November±March being the wettest months (88.9% of the annual precipitation falls) and May±September the driest months (3.3% of the annual precipitation). The warmest months are November±March (16.1±22.3 C average monthly temperatures), the coldest June±August (9.7± 14.2 C). A considerable amount of precipitation falls during the cooler period in the form of mist. Nonetheless several plants display symptoms of water de®ciency (Seguier-Guis, 1988). 2.3. Data collection Six forest fragments ranging from 0.16 ha to 136 ha and a control site of 1250 ha were investigated. For the selection of the fragments particular attention was paid to following features: . all fragments had running water, . the fragment contained no signi®cant gradients in either altitude or orientation (Fig. 1 and Table 1), . the distance of each fragment was at least 200 m from the next fragment, except for the 0.16 ha fragment which was only 100 m from two other fragments, . all study sites were located at about the same altitude (1300±1650 m a.s.l.) and

D. Vallan / Biological Conservation 96 (2000) 31±43

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Fig. 1. The ``ReÂserve SpeÂcial d'Ambohitantely'' (from aerial photographs from 1991, after Langrand, 1995). The fragments are shaded. Size of studied fragments is indicated; P=Pine or eucalyptus plantation; thick spotted line=trails or secondary roads; thin spotted line=brooks and streams.

. the increase of the surface area of the study sites was more or less exponential (0.16, 0.8, 4, 12, 30, 136 and 1250 ha). The total length of the streams in the fragments was measured on aerial photographs taken by the National Geographical Institute (FTM) in 1991. The canopy structure above the streams di€ered from the canopy

structure of the surrounding forest, and this character was discernible on the aerial photographs. These seven sites were searched along un®xed trails. Special attention was paid to amphibian biotopes (Zimmerman and Simberlo€, 1996). This procedure does not correspond to a random search of the area (Heyer et al., 1994) but provides more data. It was carried out by the same persons during the entire project (author and two

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D. Vallan / Biological Conservation 96 (2000) 31±43

Table 1 Name, size, altitude and location of the 7 study sites in the RS d'Ambohitantely Fragmenta

Size (ha)

Altitude (m a.s.l.)

Longitude (E)

Latitude (S)

Control site A0 H0 A12 H1 O22 H25

1250 136 30 12 4 0.8 0.16

1400±1650 1300±1600 1375±1550 1500±1600 1500 1500 1520

18 110 3000 18 060 0000 18 090 1500 18 060 4000 18 090 3000 18 080 4500 18 090 3000

47 170 3000 47 150 1500 47 150 4500 47 150 2000 47 150 0000 47 150 4500 47 150 1500

a

Designation after Langrand (unpublished).

local collaborators) and is, therefore, comparable across the entire study. Mark-recapture methods were not used because of the very low recapture rates of tropical amphibians (Hofer, personal communication). Collection by pitfalls with drift fences and searching of plots were discounted after a pilot study. Data were collected on anurans between mid-January and the end of March 1996 and between the end of January and the end of March 1997. Each month one or two ®eld trips of about 10 days duration were completed. During each trip each forest fragment was searched at least once by day and once by night. Each search period lasted 40 min to 3 h, depending on the size of the fragment and the same total search time was invested during the day and night. Night searches were done with torches and headlamps. Each animal found was characterised with respect to its location (height above ground, distance from the nearest water) and water type (permanent running water, temporary running water, permanent pond or temporary pond and swamps); if the frog was >10 m from one of these aquatic habitats its position was scored as far from water. To ensure that most of the species existing in each study site were being found, the search for amphibians in each fragment continued until the species accumulation curve against time reached a plateau. The searching time in each fragment varied between 22 and 90 h. Animals that could not be identi®ed in the ®eld were euthanised with ether, ®xed in 90% alcohol and preserved in 70% alcohol for later laboratory identi®cation. The specimens are held at the University of Antananarivo (Madagascar) and the Natural History Museum of Bern (Switzerland). The animals' calls were tape recorded for subsequent analysis. In cases where the presence of a species in a study site was only identi®ed by its call, the species was noted down as a single individual. To document the colour, photographs of the animals were taken. 2.4. Data analysis Data were analysed by Chi-square, Mann±Whitney test and Spearman ranking correlation test. When tied

data were present rs and Z were corrected (see Zar, 1984). In order to determine whether the loss of species in small fragments was stochastic or deterministic, the computer program ``Nestedness Temperature Calculator'' (Atmar and Patterson, 1995) was used based on presence/absence data. The calculations of this program are used to make statements on the course of the disappearance of species with decreasing fragment size. To test if the species composition and the individual frequency changes when fragment size changes, a Monte Carlo simulation was used. The six fragments (136, 30, 12, 4, 0.8, 0.16 ha) were compared with the control site. Of all individuals found in the control site, the same number of individuals as found in the fragment to be tested were randomly selected. The similarity between this simulated distribution and the observed distribution in the control site was calculated using the Canberra Metric Coecient (Krebs, 1989), which takes individual frequency into account. The probability that the species composition and the individual frequency in the fragments di€er from the one in the control site was calculated based on the observed similarity index and 1000 simulated similarity indices (Bersier and Sugihara, 1997). Two species found in the fragments on single occasions were not recorded in the control site. These two species were not used in calculating the Canberra Metric coecient because the lack of these species would lead to a non permissible division by zero. In order to quantify the e€ect of habitat fragmentation on stratum distribution of the animals, three classes were formed according to where the animals were found: (1) on the ground, (2) up to 50 cm above ground and (3)>50 cm above ground. In cases where individuals of a species were found in class 1 and class 3, or in all three classes, the sum of their relative representation in class 1 and 2, respectively in 2 and 3 was calculated. If the higher sum was less than two thirds, the species was classi®ed as intermediary: between arboreal and terrestrial (Table 1, referred to as ``a/t''). 3. Results 3.1. Species richness and density in the fragments A total of 32 amphibian species belonging to all three amphibian families known from Madagascar Ð Hyperoliidae, Ranidae (including the subfamilies Raninae, Rhacophorinae and Mantellinae) and Microhylidae (including the subfamily Cophylinae) Ð were present in Ambohitantely (Table 2). Four of these species were only found outside the rainforest (Heterixalus rutenbergi, Mantidactylus cf. alutus, M. domerguei and Ptychadena mascareniensis). Two species were found in the pseudosteppe as well as in the rainforest (Boophis goudoti and

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Table 2 Proportion of frog species found in the 7 study sites in the RS d'Ambohitantely and habitat features Species

Fragments

Horizontala habitat

Verticalb habitat

Assumedc spawning place

pw

a

iw

pw pw pw fw/pw pw fw/pw pw

a a a/t a a a a/t

iw iw iw iw iw iw iw

pw pw pw pw pw pw pw pw pw s fw pw fw pw fw/pw ps pw

t t t t t t t t t t a/t a a a a/t t a

ow ow ow ow ow ? ow ow ow ow ? ? ow ow ow ow iw

pw

a

iw

fw fw fw/pw fw fw/pw fw

a t t a a a

i i i i i i

Control A0 H0 A12 H1 O22 H25 Outside 1250 ha 136 ha 30 ha 12 ha 4 ha 0.8 ha 0.16 ha forest Hyperoliidae Ranidae

Heterixalus rutenbergi Rhacophorinae Boophis luteus Boophis ankaratra Boophis goudoti Boophis cf. brachychir Boophis reticulatus Boophis madagascariensis Boophis microtympanum Mantellinae Mantidactylus albofrenatus Mantidactylus opiparis Mantidactylus brevipalmatus Mantidactylus mocquardi Mantidactylus femoralis Mantidactylus grandidieri Mantidactylus curtus Mantidactylus betsileanus Mantidactylus biporus Mantidactylus cf. alutus Mantidactylus malagasius Mantidactylus cornutus Mantidactylus aglavei Mantidactylus peraccae Mantidactylus cf. wittei Mantidactylus domerguei Mantidactylus liber

x

1.4 0.7 2.9 0.7 3.6 0.7

1.4 11.3 12.7 4.2

3.6 8.6

1.4 2.8

1.3 1.3 5.2

1.1 1.1 1.1

1.4

2.2 7.2 4.3 12.9 2.2 15.1

5.6 4.2 1.4 2.8 4.2

2.2 0.7 4.3 18.7 1.4

14.1 1.4

0.7

21.1

2.9 12.9 4.3

2.2 4.3 2.2 9.7

1.3 13.3

1.4

14.3

3.3 3.3

5.2 6.5 5.2

4.4 13.3 6.7

9.1 29.9

7.8 21.1

3.9 5.2

3.3

1.4

6.7

31.4

1.4

2.2 3.2

17.1 10.0

8.6 7.5 11.8 12.9 9.7 4.3 28.0 4.3

6.5

1.3 4.0 12.0 44.0 14.7

Cophylinae Plethodontohyla notosticta Plethodontohyla alluaudi Stumpa sp. a Platypelis grandis Platypelis pollicaris Anodonthyla nigrigularis Species number Individual numberd

a b c d

x x

8.0

Raninae Ptychadena mascareniensis Microhylidae

x

x

x

0.7 0.7 0.7 0.7 1.4 1.4 26 139

1.4 2.8

2.6 1.3 1.3

5.6

3.9 3.9

18 71

16 77

26.7 13 90

1.3 11 70

13 93

9 75

Distance from water (horizontal habitat): pw, by permanent running water; fw, far from water; s, swamp. Vertical habitat: a, arboreal; t, terrestrial. Assumed spawning place: iw, in water; ow, near but outside water; i, independent of water, ?=unknown. No data for species recorded outside the forest.

Mantidactylus betsileanus). The other 26 species were found exclusively inside the rainforest. Hyperoliidae and Raninae were recorded outside the rainforest whereas Rhacophorinae and Mantellinae live both inside and

outside the rainforest. The Microhylids were found only inside the rainforest (Table 2). The number of species in a fragment increased logarithmically with increasing area size (Spearman, n=7, rs=0.937, P<0.01) following

36

D. Vallan / Biological Conservation 96 (2000) 31±43

the formula: S=11.00A0.108 (S=species number, A=fragment size) (Fig. 2). Only nine out of all 28 rainforest species were present in the smallest fragment while the control site contained 26 species. Two species (Boophis microtympanum and Mantidactylus brevipalmatus), only found once in two small fragments, were not found in the control site (Table 2). An increasing diversity with increasing fragment size is also indicated by the Shannon-Index (Spearman: n=7, rs=0.892, P < 0.05) (Fig. 2). Fragment size correlated positively with diversity and species richness, but negatively with the relative individual density (Spearman, n=7, rs=0.929, P=0.01). Relative density varied from 1.13 individuals found per search-

hour in the control site to 3.4 in the second smallest (0.8 ha) fragment (Fig. 3) and grew with increasing density of permanent brooks and streams (Spearman, n=7, rs=0.946, P<0.01) (Fig. 4). 3.2. Distribution of common and rare species In the control site the number of individuals of each species found varied from 1 to 26. In Fig. 5 the number of individuals recorded for a species are plotted against the number of fragments containing this species. The positive correlation (Pearson: n=28, r=0.335, P<0.05) shows that species which were rarer in the control site were likely to be found in fewer fragments.

Fig. 2. Relationship between species richness (upper line) and diversity (lower line) and fragment size.

Fig. 3. Relation between forest size and relative individual density (individuals found each searching hour).

D. Vallan / Biological Conservation 96 (2000) 31±43

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Fig. 4. Relation between permanent stream density (total length of streams per ha) in the fragments and control site and relative individual density (individuals found each searching hour).

Fig. 5. Frequency of species in the fragments depending on the relative density in the control site.

3.3. Nested subset and individual frequency

3.4. Ecological distribution of species

The analysis with the program ``Nestedness Temperature Calculator'' (Atmar and Patterson, 1995) shows that the species communities in each fragment are subsets of species of richer and larger fragments (temperature of the observed distribution: 22.07 , average of 1000 simulations: 50.93 , S.D.: 6.94 , P<0.0001). Table 3 shows that the faunal compositions (individual frequencies) of the four smaller fragments di€er signi®cantly from the control site, whereas there is no signi®cant di€erence between the two big fragments and the control site, as tested by a Monte Carlo simulation.

With increasing fragment size the proportion of arboreal species was also found to increase (Spearman: n=7, rs=0.901, P<0.02) (Fig. 6A). This ranged from 30% in the 0.8 ha fragment to 50% in the 30 ha fragment and in the control site. It also meant that the proportion of terrestrial species was negatively correlated with fragment size (Spearman: n=7, rs=ÿ0.857, P<0.05). The second smallest fragment (0.8 ha) contained the highest percentage of terrestrial species (61.5%), whereas the control site held only 38.5%. The portion of amphibian community inhabiting both lower and higher strata was independent of fragment size (Spearman: n=7, rs= 0.091, ns).

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Table 3 Probability that the species composition and species frequency in the fragments are the same as in the control site (for explanations see text) Fragment size (ha) 136

30

12

4

0.8

0.16

Number of simulations (n=1000) 627 364 0 2 1 0 less similar to the control site than the observed Probability P (one-tailed) 0.627 0.365 0.001 0.003 0.002 0.001

3.5. Stream density in the fragments and dependence of amphibians on water Fragments in RS d'Ambohitantely persist only near streams (see section ``Study area''), especially the smallest ones. In the larger fragments rainforest also extends over greater distances between streams. Correspondingly the proportion of streams per area (m/ha) decreased with increasing fragment size (Spearman: n=7, rs= ÿ0.964, P<0.005) (Fig. 4). Amphibians were found in all ®ve water-related habitat types (Table 4): 81.2% of all individuals were found near permanent running waters, 12.3% were found far from water. Temporary running waters, permanent ponds, temporary ponds and swamps contained fewer animals. At the species level the situation was similar: most species (82.1%) were found near permanent running waters, 57.1% of the species were found farther than 10 m from any aquatic habitat and 25% were observed near temporary running waters. The other three aquatic habitats (permanent pond or temporary pond and swamps) contained few amphibian species (Table 4). This re¯ects the frequency of the water-related habitats in the fragments rather than the species' preferences. To compare the ®ve aquatic habitats, three classes were constructed that contained at least two thirds of all individuals of a species: (1) closer than 10 m to a permanent running water (17 species), (2) far from water (6 species) and (3) indi€erent to water proximity (5 species) (Table 2). Fragment size had no signi®cant in¯uence on the portion of species living both near and far from permanent running waters (Spearman: n=7, rs=0.685, P<0.2) (Fig. 6B). Furthermore, there was no signi®cant correlation Ð only a tendency Ð between fragment size and species found near permanent running waters (Spearman: n=7, rs=ÿ0.612, P<0.2). With increasing fragment size the portion of species living far from water increased (Spearman: n=7, rs=0.788, P <0.05). This group of frogs occurred only in fragments of 30 ha or more. Concerning the proximity to water there seems to be more of a step relationship than a linear relationship (Fig. 6B): there are signi®cant di€erences between the four smaller and the three larger fragments of all three classes (closer than 10 m to a permanent running water:

Fig. 6. Natural history traits of anurans in relation to fragment size: (A) Proportion of arboreal and terrestrial species in the fragments: *=terrestrial species, ~=arboreal species and ^=terrestrial and arboreal species. (B) Dependence of the species on permanent running water: ^=percentage of species found <10 m from permanent running waters, ~=percentage of species found >10 m from permanent running waters and *=percentage of species found both near and far from permanent running waters. (C) In¯uence of fragment size on spawning site: *=spawning outside water, ~=spawning in water and ^=reproductive strategy independent of water.

Table 4 Species and individual numbers found near ®ve aquatic habitats and far from aquatic habitats in all fragments and the control site Number of individuals (%) <10 m from permanent running water <10 m from temporary running water <10 m from permanent standing water <10 m from temporary standing water In a swamp >l0 m from water

Number of species (%)

493 (81.2)

23 (82.1)

12 (2.0)

7 (25.0)

7 (1.2)

3 (10.7)

4 (0.7)

1 (3.6)

13 (2.1) 78 (12.3)

3 (10.7) 16 (57.1)

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Mann±Whitney test: Z=ÿ1.962, P<0.05; far from water: Z=2.145, P<0.05; both near and far from permanent running waters: Z=1.980, P<0.05). 3.6. Spawning site Reproductive strategies of the Ambohitantely frogs can be divided into three groups. (1) Species spawning directly into water (Rhacophorinae). (2) Species spawning outside water, on leaves, branches or stones above or near water; The larvae will be ¯ushed into water after embryogenesis (Mantellinae). (3) Species independent of running waters or ponds for spawning (most Microhylidae). These latter species spawn into water-®lled tree holes or bamboo internodes or have a water-independent direct development (Table 2). Nothing is known about the reproduction of Mantidactylus malagasius, M. cornutus and M. grandidieri. As the proportion of amphibian species living far from water increased, so did the number of amphibians species having a water-independent reproduction strategy (group 3) (Spearman: n=7, rs=0.775, P<0.1) (Fig. 6C). The number of species spawning outside water (group 2) tended to decrease with increasing fragment size (Spearman: n=7, rs=ÿ0.685, P<0.2), but the fragment size had no in¯uence on the proportion of amphibian species spawning directly in water (Spearman: n=7, rs=ÿ0.071, P>0.5). Concerning the spawning place there again seems to be rather a step than a linear relation (Fig. 6C). The frequency of species spawning outside water was higher in the four smaller fragments than in the others (Mann±Whitney test: Z=ÿ2.018, P<0.05). Conversely the frequency of species independent of running waters or ponds for spawning was less high in the four small fragments (Mann± Whitney test: Z=1.962, P<0.05). No di€erence was found between the four small and three large fragments for species independent of running waters or ponds for spawning (Mann±Whitney test: Z=ÿ0.530, ns). 3.7. Taxonomic composition There were no signi®cant di€erences between the distribution of the families and subfamilies in the fragments (a2=5.443, df: 12, ns), but it was obvious that fragments < 30 ha lacked microhylids (Table 2) apart from one juvenile Platypelis pollicaris found in the 0.16 ha fragment. 4. Discussion 4.1. E€ects of fragmentation on species richness Following the expectations founded on the theory of island biogeography (MacArthur and Wilson, 1971), the species number of amphibians in rainforest fragments

39

increased logarithmically with area (Fig. 2). This was previously shown in various studies [e.g. Zimmerman and Bierregaard, 1986 and Tocher et al., 1997 (amphibians); Newmark, 1991 and Langrand and WilmeÂ, 1997 (birds) and Goodman and Rakotondravony, in press (mammals). The Ambohitantely amphibian community within the fragments formed a clear nested subset, and thus the reduction of species richness as a function of forest size was not stochastic. Species showing small populations in the control site are the ones most likely to disappear from small fragments (Fig. 5) (Newmark, 1991). This is not so surprising given that small populations are most threatened by extinction. They react more sensitively to genetic, demographic and environmental ¯uctuations than large populations (Sha€er, 1981; Gilpin and SouleÂ, 1986; Soule 1987). Laurance (1991) observed that for mammals it is not the frequency in the original habitat but the frequency in the matrix which is critical for the species' survival probability. As the predominant pseudosteppe matrix in the research area is unsuitable habitat for most amphibians, this hypothesis does not apply to the present study. Yet, it must be mentioned that both species that are found in the rainforest as well as in the matrix (Boophis goudoti and Mantidactylus betsileanus) have consistent population levels in nearly all fragments and probably move regularly between forest and pseudosteppe. The other four species found in the matrix (Heterixalus rutenbergi, Mantidactylus cf. alutus, M. domerguei and Ptychadena mascareniensis) were not found in the fragments or in the control site, and thus may well be specialists of non-forested habitat. 4.2. Vegetation structure, edge e€ect and microclimate As we have seen above, the population size in the intact habitat is not the only determining factor for the survival of a population in fragmented habitats. Amphibians often display a patchy distribution (e.g. Zimmerman and Bierregaard, 1986) and are mostly bound to certain microclimatic conditions or spawning places. If the conditions of a species are not met, they cannot persist. The larger a rainforest fragment is, the more likely it will contain di€erent microhabitats. The four forest types described by Rajoelison (1990) and Razakanirina (1993) were only found in the control site. The smaller the fragment, the more homogeneous was its vegetation structure. As an example for this point, the Microhylidae were found practically only in the slope forest and if no such forest type occurred within the fragment, the number of species of Microhylidae decreased rapidly. Fragments are exposed to the climate of the surrounding habitat (pseudosteppe). The microclimate on the edge of fragments showed higher temperature, lower atmospheric and soil humidity and stronger winds than did the core area (Kapos, 1989; Saunders et al., 1991;

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Murcia, 1995). These conditions are adverse to amphibians (Pough et al., 1977) and can show e€ects up to 100 m into a fragment (Saunders et al. 1991). Species which do not live near water (most Microhylidae, Mantidactylus malagasius and M. aglavei) are handicapped in smaller fragments, in which the edge e€ect in¯uences the whole fragment leaving no unin¯uenced core area. Correspondingly, the occurrence of these species increased with fragment size (Fig. 6). Apparently, microhylids need fragments with a minimal size of 30 ha, at least in a climatic zone and rainforest vegetation comparable to Ambohitantely. In the lowlands of Madagascar microhylids seem to be less sensitive to the e€ect of habitat fragmentation (Vallan, unpublished). This may be correlated with the distinct climatic change of seasons in the highland. Stream-dwelling, often semi-aquatic species (many mantellines), can probably better endure the adverse microclimatic conditions of small fragments. This may be due to the fact that they can cool themselves in the water and absorb humidity. These species (Mantidactylus mocquardi, M. femoralis, M. grandidieri, M. curtus, M. betsileanus and M. biporus) were also found in the smaller fragments, and all Ð except M. grandidieri and M. biporus Ð were present even in the smallest fragment. Most species and individuals in the rainforest of Ambohitantely lived near streams (Tables 2 and 4). Because the density of streams correlates inversely with the size of fragment (Fig. 5), it is not surprising that the proportion of species that live near water decreases with increasing fragment size. 4.3. Amphibian density With decreasing fragment size the individual density can increase. One explanation for this would be the crowding e€ect described by Bierregaard and Lovejoy (1989) for birds that retreat to the remaining rainforest fragments when this habitat is cleared. However, this is a short-term e€ect, and after a while the individual density decreases again (Askin et al., 1987). The fragmentation of the intact rainforest in Ambohitantely took place in the last few centuries, so a temporary crowding e€ect can be discounted. The increase in individual density in smaller fragments is probably due to the higher density of brooks and streams in these fragments and the

majority of individuals living near streams (Fig. 4). The fact that the forest remnants in Ambohitantely are mostly located near brooks and streams is probably due to the sensitivity of plants toward austral winter drought. Small fragments usually consist of forest area surrounding brooks. In larger fragments the forest extends over long distances between brooks and streams. In the forest there are only six amphibian species which occur at large distances from open water (Table 2), but they made up only a small part of all individuals found (Table 4). 4.4. Species diversity in Ambohitantely in comparison to other mountain rainforests In addition to the 32 amphibian species found during this study in RS d'Ambohitantely, two additional species (Boophis boehmei and B. cf. rhodoscelis) were documented during a visit to the site in April 1995 (Glaw and Vallan, pers. obs.). Seguier-Guis (1988) found additionally the following ®ve species (out of a total of 14) during her studies in the same area: Mantella betsileo, Mantidactylus plicifer, M. aerumnalis, B. untersteinii and Anodonthyla boulengeri. I have been unable to ®nd voucher specimens for these records and they must be evaluated on distributional and taxonomical information. Boophis untersteinii is now regarded as a synonym to B. goudoti (Glaw and Vence, 1994). A. boulengeri is extremely similar to A. nigrigularis, which has been described by Glaw and Vences in 1992. They are distinguished mainly by their call (Glaw and Vences, 1992). M. aerumnalis possibly refers to M. brevipalmatus (Glaw, pers. comm.). Glaw and Vences (1994) also mention Mantidactylus albolineatus, M. punctatus and M. ambohimitombi as occurring in Ambohitantely based on data from Blommers-SchloÈsser and Blanc (1991). Thus all in all, the nature reserve of Ambohitantely harbours at least 36 anuran species. In Table 5 the richness of forest-dwelling species of the RS d'Ambohitantely is compared with those of Anjozorobe (the nearest rainforest at a similar altitude) and another four mountain rainforests [Andringitra, Montagne d'Ambre, Anjahanaribe-Sud (east and west)]. Frog species richness at Ambohitantely does not deviate strongly from those of the other large rainforest blocks, indicating that a relatively small nature reserve with a contiguous forest block of 1250 ha is sucient to harbour

Table 5 Number of amphibian species found in other humid montane forests of Madagascar at similar altitude as Ambohitantely Site Ambohitantely Anjozorobe Andringitra Montagne d'Ambre Anjahanaribe-Sud (east) Anjahanaribe-Sud (west)

Altitude (m a.s.l.)

Number of rainforest species

1300±1650 1300 1200±1700 1150±1300 1100±1700 1200±1600

28 23 29 14 36 21

References Present study Raselimanana (1998) Raxworthy and Nussbaum (1996) Raxworthy and Nussbaum (1994) Raxworthy et al. (1998) Raxworthy et al. (1998)

D. Vallan / Biological Conservation 96 (2000) 31±43

a high amphibian species diversity. In contrast to amphibians, birds seem to react more sensitively to habitat size reduction as shown by Ravokatra et al. (1998): compared with Anjozorobe, Ambohitantely has a clearly impoverished avifauna. 4.5. Sensitivity of various taxa to fragmentation In the RS d'Ambohitantely, the z-value which re¯ects the sensitivity of a taxon to fragmentation-related factors, was found to be 0.108 (Fig. 2). This is at the lower limit set by MacArthur and Wilson (1971) for habitat fragments on ``mainlands''. In the RS d'Ambohitantely the z-value is 0.159 for birds (Langrand and WilmeÂ, 1997), 0.224 for insectivorous (Goodman and Rakotoandravony, in press) and 0.268 for reptiles (Vallan, unpublished data). Abbott (1983) pointed out that the z-value is a product of various factors. Species with large home-ranges need larger areas of habitats than those with smaller home-ranges. The z-value depends also upon the ability of species to migrate between the fragments, therefore the degree of isolation of a fragment also contributes to the z-value. Owing to the fact that this study was done in the same area as Langrand and Wilme (1997) and Goodman and Rakotondravony (in press) and to a large extent in the same fragments, the degree of isolation may be disregarded when comparing the z-values. The measured di€erences between these four di€erent classes of vertebrates is therefore probably based upon their di€erent sensitivity to fragmentation and their migration abilities. It appears that insectivores, reptiles and birds react more sensitively to habitat fragmentation than amphibians. Either birds, reptiles and insectivores have higher requirements concerning minimum fragment size than amphibians, or the matrix between the fragments represents a more insuperable barrier for them than for amphibians. I suppose that due to the sensitivity of amphibians to dryness and high temperature, the pseudosteppe between the fragments is an even larger obstacle for amphibians than for birds and small mammals. Therefore, it can be concluded that amphibians are less sensitive to fragment size than birds, reptiles or insectivores. 4.6. Implications for conservation Due to early deforestation it is dicult to say what the original amphibian fauna of Madagascar's highland plateau was. Nevertheless the comparison with other, widely extended Malagasy rainforests of similar altitude (see Section 4.4) shows that, to protect amphibian species, nature reserves of at least 1250 ha would be appropriate; these will contain a considerable part of the original species richness. It is quite possible that an impoverishment of the anuran fauna in Madagascar's highland took place. Several species (Mantella betsileo,

41

Mantidactylus plicifer, M. aerumnalis, Mantidactylus albolineatus, M. punctatus and M. ambohimitombi) mentioned as existent in the RS d'Ambohitantely have not been found during this research project (see Section 4.4). Although this might have been due to natural ¯uctuation, it is nevertheless worth mentioning that all these species belong to the subfamily Mantellinae, a mainly terrestrial taxon. As shown by Pough et al. (1998) terrestrial anurans are often more sensitive to dryness. Consequently, species of the subfamily Mantellinae and Microhylids (see Section 4.2) can be used as bioindicators due to their sensitivity to microclimate changes. It is not only the size of a protected area that is decisive for species and individual richness. This also depends on the shape (microclimate), the richness of structures they contain and ± especially for anurans ± also on the water bodies contained. It follows that an area containing a rich mosaic of various vegetation types and abiotic structures can be much more valuable for species protection than a larger but less structured one provided that the area is large enough to contain a stable population of the species or the community in question. Acknowledgements I thank Frank Glaw and Franco Andreone for all their help during the study. I am very grateful to Wolfgang Nentwig, Steve Goodman, Olivier Langrand, PieÁrre Berner, Walter HoÈdl, Sven Bacher, Claudio Vallan and Markus Frischknecht for all the fruitful discussions and suggestions. Thanks also to Solofo and Armand for the help in the ®eld, to Natalie Baumann-Stadelmann for the translation of the script and to the two referees and the editor for the review of this article. The research in Madagascar was made possible by scienti®c cooperation with the University of Antananarivo, the ®nancial support of the Swiss Academy of Natural Sciences (SANS) and the Natural History Museum of Bern. The research was also supported by Air Madagascar, Photo-Wyss (ZuÈrich) and Tramp Store (Trimbach) and authorized by the Direction des Eaux et ForeÃts (DEF), Association National pour la Gestion des Aires ProteÂgeÂes (ANGAP), and the Commission Tripartite.

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