J. South Asian nat. Hist., ISSN 1022-0828. February, 1996. Vol.2, No. 1, pp. 1-30,12 figs., 13 tabs. © Wildlife Heritage Trust of Sri Lanka, 95 Cotta Road, Colombo 8, Sri Lanka.

Resource use and foraging tactics in a south Indian amphibian community

Indraneil Das*

Abstract This study looks at resource (trophic, spatial and temporal) use and foraging tactics in a community of eight species of anuran amphibians at a seasonal locality in south India. Within the community, the species are differentiated into a sit-and-wait group, which are large, cryptic and sedentary foragers showing a relatively wide dietary spectrum; and a widely foraging group, whose members are aposematically coloured, and actively forage on a few prey types. However, there are indications that these modes represent ■ two ends of a continuum, with some species showing greater plasticity in prey use than others. Sympatric species, except dietary specialists, were found to generally overlap broadly in diet. Microhabitats are partitioned to a greater degree than food, the most closely related species, which tend to show similar diets, selecting different foraging areas. Seasonality affects the activity of two of the three non-sit-and-wait species, but none of the sit-and-wait ones, possibly because sedentary foraging is more energetically effi­ cient during the resource lean season. Net gains per unit energy spent are presumably lower than for active foraging. In general, both trophic and spatial niches increase in breadth with body size across species, with larger species taking more types of food and using more different microhabitat types than smaller ones. Smaller species take smaller prey, but the mean number of prey harvested is higher than in larger frogs. Differences in the use of envi­ ronmental resources are thought to be a factor in determining species composition in a community, within which larger species tend to be generalists, while their smaller sympatrics are more specialized in their use of environmental resources.

Key words: resource use, community, niche, foraging, amphibians.

* Animal Ecology Research Group, Department of Zoology, University of Oxford, South Parks Road, Oxford 0X1 3PS, United Kingdom. Present address: Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cam­ bridge, MA 02138, USA. DAS

Introduction Ecological differences in the use of trophic (food), spatial (place) and temporal (time) resources have long been associated with the structure of biological coifi- munities because of their potential to reduce competition/ thereby apparently facilitating coexistence (Pianka, 1975). Amphibians and reptiles exploit adaptive zones based on low energy flow that are unavailable to endothermic tetrapods, because their modest energy requirements allow the exploitation of niches not used by birds and mammals (Pough, 1980). Niche relations among these groups of animals are thus wor­ thy of study, particularly because most of the current theories on vertebrate community-structure are derived from investigations on avian and terrestrial mammalian communities (but see the works on saurofaunas, reviewed by Pianka, 1986; and a review of resource partitioning patterns in herpetofaunal communities, by Toft, 1985). Among amphibians and reptiles, anurans are undoubtedly the most speciose group (approximately 4,000 described living species), and compose a major component of the vertebrate faunas in many parts of the world. Relatively few community-level studies have been directed at adult frog assemblages, most of these being conducted in the New World tropics (e.g., Duellman, 1978, 1989; Toft, 1980, 1980a, 1981). Studies on the Asian fauna have been rarer still, all conducted by Robert Inger and co-workers, in Thai­ land (Inger and Colwell, 1977), Sarawak, Malaysian Borneo (Inger, 1969) and the Western Ghats forests of south-western India (Inger et al., 1987). This paper is based on an eighteen-month field study on patterns of re­ source use and foraging tactics in a community of eight anurans at a seasonal locality in south India. Study area Field work was conducted in Chengai-MGR (formerly Chengleput and Chengai) District, Tamil Nadu State, south India, centred around the village of Vadanemmeli (12° 45'N; 80°12/E), approximately 42 km south of the city of Madras, on the south-east coast of India. The area is a stretch of coastal scrub­ land, interspersed with a large number of permanent or ephemeral water bod­ ies. Most of the waterbodies are along a 1.25 km stretch of low-lying land, in an almost continuous series. Three broad categories were identified, based on surface area and permanency: Large permanent (N=2), 1326-2728 (mean 2027) m2, small permanent (N=4), 1.0-27.5 (mean 8.5) m2, and ephemeral (N=4), 302.5- 1210.0 (mean 759) m2. The mean maximum depth of these bodies of water varies between 3.0 m for the large permanent ponds, through 1.5 m for ephem­ eral ponds, to < 1.0 m for the small permanent bodies of water that are exca­ vated by the human residents to entrap rainwater. All measurements of sur­ face area and greatest depth were made during the peak of the Southwest monsoons, and depth of the large permanent waterbodies was observed to vary greatly seasonally. A variety of aquatic macrophytes and riparian veg­ etation occur in association with the larger waterbodies, including submerged (Ceratophyllum demersum, Vallisneria spiralis, Hydrilla verticillata, Phyla nodiflora, Alysicaiyns manilifer, Ottelia alismoides, Oedogonium sp. and Zygnema sp.), float­ ing (Nymphaea stellata and Lemna perpusilla) and emergent (Aponogeton natans)

2 J. South Asian nat. Hist. R eso u r c e u s e a n d fo r a g in g ta ctics in s o u th In d ia n a m ph ibia n s types. The sedge Cypenis sp. frequently forms the major vegetation of the shores of the permanent waterbodies, while the ephemeral ones have barren shores, o Other major amphibian habitats include Casuarina forests, which are ex­ tensive on the seab^aches and typically lack undergrowth. Human habita­ tions also occur in the area and comprise thatched huts and a few concrete structures. An eight acre area of land belonging to the Madras Crocodile Bank Trust, which has been carefully planted with many local tree species, espe­ cially neem (.Azadimchta indica), is the most densely vegetated patch at the site. Mean daily maximum and minimum ambient temperatures for the hottest (May-June) months are 36°C and 28°C, respectively; corresponding figures for tih.e coldest months (December-January) being 29°C and 21 °C, respectively. The dry season is long, extending for about four months from February to mid-June. This is followed by the summer monsoon which extends until Sep­ tember, but brings comparatively less precipitation than the winter monsoons, which occur between the end of October and mid-December. The area received 1147 mm of rainfall in 1989, the figures for the following year being 47.7% greater (1694 mm), which can be attributed to a cyclone which hit the area in May. Study species Eight species of anuran amphibians occur at the study site— Indian green frog, Rana hexadactyla (Lesson, 1834). Unique among anuran am­ phibians in being primarily folivorous throughout adulthood, the frog feeds on a variety of aquatic macrophytes. This is the largest as well as the heaviest species in the study site, attaining 132.2 mm in snout-vent length and weigh­ ing up to 270 gm. Newly metamorphosed frogs, between about 15-30 mm snout- vent length feed on various kinds of insects. The species is restricted to the comparatively deeper (> 2 m depth) waterbodies. Jerdon's bullfrog, Rana crassa (Jerdon, 1853). This species attains 93.1 mm in snout-vent length in the study site and inhabits the edges of ephemeral waterbodies, where they sit in wait for invertebrate, and very occasionaly, small vertebrate prey. Skipping or skittering frogs, Rana cyanophlyctis (Schneider, 1799). Two distinct colour morphs occur in the site, a dark-blotched, large-sized (to snout-vent length 70.7 mm) form that inhabits permanent ponds, and an unpatterned, small (to 40 mm) form restricted to temporary ponds. Aquatic insects, espe­ cially beetles, constitute the mainstay of the diet of this species. South Indian burrowing frog, Tomopterna rolandae (Dubois, 1983) . Encountered in the Casuarina forests and agricultural fields especially during the rains, the species reaches a snout-vent length of 43.2 mm and forages on beetles and many other groups of invertebrates. Marbled balloon frog, Uperodon systoma (Schneider, 1799). A secretive and prob­ ably rare species that is encountered only during rainy nights, at the height o f the monsoons. The species reached 54.7 mm in snout-vent length and special­ izes on termites and ants.

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Red narrow-mouthed, frog, Microhyla rubra (Jerdon, 1854).. A relatively com­ mon, brightly coloured ant and beetle specialist, this species reaches a snout- vent length of 26.5 mm. Ornate narrrow-mouthed frog, Microhyla ornata (Dumeril & Bibron, 1841). A rather rare species in the study area and a small insect-specialist. This species attains only 17.4 mm, making it the smallest frog species in the study site. Common Indian tree frog, Polypedates maculatus (Gray, 1834). With microhabitat requirements quite different from those of the species already described, the common Indian tree frog rests on trees or inside human habitations during the day, emerging after dark to forage on the ground or on trees. In the dry season, activity is greatly reduced, when it hides under leaf sheaths of banana trees, and may also take shelter in cracks inwalls inside human dwellings. This spe­ cies attains a snout-vent length of 79.2 mm. Its broad diet includes both verte­ brate and invertebrate prey.

Methods Data on which this paper is based were obtained between March-August and November-December, 1989, and January-December, 1990. Only frogs (meta­ morphosed individuals) have been considered. Frogs were caught during all periods of the day using a variety of techniques, including dip-nets, by hand or by "angling" with hooks, depending on the activity, behavior and microhabitat type of the species. The microhabitat and time and date of cap­ ture were noted. Specimens were brought to the laboratory and sacrificed within three hours of capture in order to obtain data on stomach contents. To examine the degree of dominance of food items in stomach samples, the Berger-Parker Diversity Index was used—

where N is the total number of individuals and Nmax , the number of individu- als in the most abundant resource type. The reciprocal form of the measure was used so that the index increases with increasing prey diversity (Magurran, 1988). Since the data are based on non-random (stomach) samples, the monthly changes in the diversity of prey were estimated using the Brillouin Index (see Magurran, 1988, for justification)—

HB = In N! - 2 In nil N where ni represents the number of individuals in each prey resource state; N, the total number of individuals in all resource states, and ! represents a facto­ rial. To calculate factorials for N >10, Sterling's slacker approximation (In N! ~ nlnN-N) was used (Whittaker and Watson, 1963). Niche breadths of the eight sympatric species were estimated using the Shannon-Weiner Index of Diversity (see Inger et al., 1987)— H' = -2pi Inpi

J. South Asian nat. Hist. R eso u rce u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s where pz represents the proportional abundance of the species found utilizing the i th resource state. Niche overlaps between the eight species were calculated using a symmet­ ric version (fide Pianka, 1986) of MacArthur and Levins' (1967) equation—

Spy ?ik V 2pz)’2 -pile2 where pi/ and pik are the proportions of the zth prey resource state used by the /th and M i species. The overlap may theoretically vary between zero (no over­ lap or dietary similarity) to one (total overlap or completely similar diet). Dietary analyses are based on ordinal level of prey identification. Compu­ tations of niche breadths, niche overlaps and dominance were made from data after compilation into a rectangular in by n matrix that indicates the rate of utilization of each m discrete resource type (food or microhabitat) by n anuran species. Cluster analyses were conducted using SYSTAT, version 5.03 (Wilkinson, 1990).

Abbreviations: HW (head width, measured at the angle of the jaws); SVL (snout-vent length, measured from the tip of snout to the vent) and PL (great­ est prey length). Three measures of prey size, all log-transformed, were used to examine the scaling of prey size to frog head width, including PLMAX (the length of the largest intact prey item found in a stomach); PLX (the mean length of all intact items in a stomach) and PVMAX (the volunj£ of the largest intact prey item in a stomach; estimated by displacement of wat£r fri graduated cyl­ inders), the last measure is only used for the large-prey eaters, since the vol­ ume of individual prey items could not be assessed accurately for the small prey eaters, including Microhyla ormta, M. rubra and Uperodon systoma. Results Diet Size Relationships with prey. A summary of the statistics of length of prey ingested by the eight sympatric anuran species at the study site has been pro­ vided in Table 1. Polypedates maculatus exhibits the strongest correlation between head width and prey size, r=0.936 (PLX, since the raw data in this particular species com­ prise only one item) and 0.917 (for PVMAX), all correlations significant (P < 0.05). This species selects large prey. The highly positive relationship of prey size with head width, here considered an index of gape, suggests that prey selected is as large as possible within mechanical limits. The value of the slopes (&) of the regressions between HW and PLMAX (and PLX) and PVMAX were 3.13 and 3.91, not significantly (f-tests, P > 0.05) greater than required for isometry (b=1 for PLMAX and PLX; 3 for PVMAX; see Gould, 1966, for justifi­ cation). These results indicate that although the regression coefficients may not differ significantly from isometry, larger frogs take larger prey than smaller ones, the increase in head width during ontogeny presumably helping to par­ tition food intraspecifically.

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Table 1. Prey size (cm) and number of animal prey per stomach in the eight anuran species. Abbreviations:—(1): species, Mo, Microhyla omata; Mr, M. rubra} Tr, Tomoptema rolandae; Us, Uperodon systoma; Pm, Polypedates maculatus; Rc, Rana cyanophlyctis} Rcr, R. crassa; Rli, R. hexadactyla. (2), N; (3), range; (4), x±SE; (5), variance, v; (6), coefficient of variation, cv; (7), N; (8), range; (9), x±SE; (10), variance, v; (11), coefficient of variation, cv.

Prey length Prey items (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11) Mo 8 0.30- 0.46 (0.353 ± 0.018) 0.003 14.366 4 2-5 (3.25 ± 0.629) 1.583 38.717 Mr 22 0.21- 0.56 (0.298 ± 0.0176)0.007 27.696 4 1-17 (6.00 ± 3.786) 57.333 126.198 Tr 182 0.18- 8.10 (0.528 ± 0.054) 0.528137.592 10 I-37 (8.6 ± 3.403) 115.822 125.140 Us 358 0.20- 0.56 (0.317 ± 0.003) 0.004 20.143 4 II-235(95.2 ± 53.1) 9421.583 110.615 Pm 5 0.41- 6.30 (3.130 ± 1.26) 8.410 94.829 5 1-2 (1.2 ± 0.20) 0.2000 37.268 Rc 89 0.10-2.65 (0.847 ± 0.060) 0.323 67.156 45 1-17 (3.356± 0.46) 9.507 91.888 Rcr59 . 0.19-4.36 (1.040 ± 0.097) 0.555 71.823 33 1-10 (2.758± 0.389) 5.002 81.104 Rh 224 0.01-7.13 (1.543 ± 0.111) 2.739107.259 92 1-33 (3.293+ 0.495) 22.583 144.291

An examination of the data on the relationships between PLMAX and PLX to HW for the rest of the study species fails to reveal any pattern. Large-prey eaters (includingRana cyanophlyctis, R. crassa and R. hexadactyla), r=0.283-0.658, as well as the small prey eaters (Microhyla rubra and Uperodon systoma), 1-0.480- 0.860, showed weak or no correlation, as did the dietary generalist Tomoptema rolandae, r=0.452 (PLMAX) and 0.549 (PLX), suggesting that both large and small prey items maybe ingested at a given gape size in these ecological groups. Mean prey length, when regressed with mean SVL or mean HW, on log-log paper, shows a linear relationship (Figs. la and lb), with both correlations be­ ing positive (r=0.748 and 0.778, respectively). The slightly stronger correlation with HW is predictable, because prey capture and manipulation is accomplished primarily with the mouth in anurans. However, a significant departure from the general trend is shown by the fifth largest species in the community,

a b

log-x SVL log-x HW Figure 1. (a) Relationships between mean snout-vent length (mean SVL) and mean prey length (mean PL); (b) mean head width (mean HW) and mean prey length (mean PL) in the eight anuran species, arranged in a size-series, from the smallest (Microhyla omata) to the largest (Rana hexadactyla) on log-log scale.

J. South Asian nat. Hist.

■ R eso u r c e u se a n d fo r a g in g , ta ctics in so u th In d ia n a m ph ibia n s

Uperodon systoma, which feeds on prey comparatively small for its body size. The frequency of prey in each size-category that are utilized by the eight sympatric species at the study site have been represented in Fig. 2 . Most spe­ cies show a unimodal peak which indicate that more smaller prey items are ingested than expected. Clear exceptions include Polypedates maculatus, ap­ parently an opportunistic forager that ingests proportionately many more large prey than any of its sympatrics, and Rana hexadactyla f which shows a trimodal peak in prey usage, although the larger prey items are only ingested by female adults prior to egg production (Das, 1996). Between the eight sympatric spe­ cies at the study site, prey length showed significant statistical differences (one­ way ANOVA, F7/943=43.371, P < 0.001). Peters (1983) found large-prey eaters to be more variable in their prey choice than small-prey eaters, presumably since small prey (chiefly ants and termites, in this study) are likely to show less variance in size than larger prey, such as vertebrates and some of the larger invertebrate taxa, including molluscans, crustaceans, oligochaetes and chilopodans. In addition, all other things being equal, large-prey eaters can feed on a wider prey-size range than small-prey eaters: increasing body size appears to help broaden the range of prey size ingested by the frog species. Since mean prey length bears a positive relation­ ship to both the size of the predator and the organ associated with prey cap­ ture (here mouth, or HW measured across the jaws), the relationship between mean HW and the coefficient of variation of prey length was expected to be positive. The result (Fig. 3) reveals extensive scatter (r=0.310), and this corre­ lation is not significant (P > 0.05). The data above (from Table 1) do show that larger frogs tend to have larger cv, the w;eak correlations being the result of the tendency of some species to show lower (e.g., Uperodon systoma) or higher (e.g., Tomopterna rolandae) cv than would have been expected from head width alone. Within the community, the highest cv (137.59) was found in the wide­ mouthed dietary generalist, Tomopterna rolandae, which feed on a wide size range of invertebrate prey, and the lowest (14.37 and 20.14) in the narrow­ mouthed dietary specialists (.Microhyla ornata and Uperodon 'systoma) that feed principally on ants, termites and small beetles. Similar patterns (weak corre­ lation between variation in prey length and frog size) have been reported from a Bornean rainforest anuran community by Inger (1969), and suggest that larger frog species in the study area are more variable in their choice of prey size (which are also statistically expected to show greater variance than small prey), being capable of preying on a wider size-range than smaller frog species, all of which show narrower diets, taking fewer prey groups. If the eight species were divided into two foraging groups, the sit-and- wait (SW; including Rana cyanophlyctis, R. crassa, R. hexadactyla, Polypedates maculatus and Tomopterna rolandae) and non-SW (including the widely-forag­ ing, WF, Microhyla ornata and M. rubra, and also Uperodon systoma, which shows an unusual foraging strategy, see 'Discussion') predators, the cv of prey length (data from Table 1) of SW species is significantly (£-test, P < 0.05) larger than in species not practising this foraging mode. This is expected, since frogs show­ ing the SW mode are presumably less discriminate in prey choice, whereas WF frogs (as well as U. systoma) actively search prey, selection of food presum-

Vol. 2., No. 1. 7 Figure 2. Prey-length distribution in the eight anuran species.anuran eight the in distribution Prey-length 2. Figure 8 NO. OF ITEMS NO. OF ITEMS NO. OF ITEMS NO. OF ITEMS m - n 'TT r r n i t i t i"i"i"it | n r-n T r-n | n i"i"i"it t i t i n r 'TTr n - m RYS2 CLASS PREY-SI2E PREY-SIZE CLASS PREY-SIZE CLASS PREY-SIZE CLASS Polypedates maculatus 1 3232222223333333 PREY-SIZE CLASS RYSZ CLASSPREY-SIZE PREY-SIZE CLASS PREY-SIZE CLASS : J.South Asian nat. Hist. D AS R eso u r c e u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s

Table 2. Hutchinsonian ratios of head width (HW) and prey length (PL) (mean values for each species divided by corresponding values for adjacent species); percent incre­ ment of HW and PL. Mean HW and PL in cm.

Head width Prey length Species X Ratio Increment x Ratio Increment Microhyla ornata 0.41 - - 0.35 - - Microhyla rubra 0.72 1.76 75.61 0.30 0.86 -14.29 Tomopterna rolandae 1.09 1.51 51.39 0.53 1.77 76.67 Uperodon systoma 1.24 1.14 13.76 0.32 0.60 -39.62 Rana cyanophlyctis 1.61 1.30 29.84 0.85 2.66 165.63 Polypedates macidatus 2.09 1.30 29.81 3.13 3.68 268.24 Rana crassa 2.29 1.10 9.57 1.04 0.33 -66.77 Rana hexadactyla 3.34 1.46 45.85 1.54 1.48 48.08 ably being made largely on the basis of size alone. Variation in prey length is therefore expected to be less in the non-SW species. Ratios for the linear body dimensions in the study species and their prey have been presented in Table 2, the mean value for HW being 1.37, when spe­ cies are arranged according to body size. However, no apparent pattern of increment in the increase in PL between adjacent species could be detected, presumably because of the tendency of Uperodon systoma to take prey much smaller than expected for its head width and of Microhyla ornata to ingest rela­ tively large prey. Hutchinsonian Ratios of prey length (mean prey length for each species divided by corresponding value for adjacent species) were estimated for frogs in the study site (Table 2). Species were also divided into two broad ecological groups (Table 3) that probably represent true guilds (or functionally similar species within a community, sensu Root, 1967), or perhaps more accurately "taxon guilds", comprising closely-related species, the members of which prob­ ably belong to a larger guild (see Schoener, 1986): a group comprising strictly terrestrial species (comprising Microhyla ornata, M. rubra, Uperodon systoma and Tomopterna rolandae) and an aquatic/semi-aquatic group (including Rana cyanophlyctis, R. crassa and R. hexadactyla). Excluded from these analyses is Polypedates macidatus, which forages in microhabitats different from those of

150

0 100 1 0 | 1 50 o

Figure 3. Relationships between mean 0 headwidth (mean HW) and the coeffi­ cient of variation of prey length in the x HW eight anuran species.

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Table 3. Hutchinsonian ratios of prey length (PL) [mean values for each species divided by corresponding values for adjacent species] and percentage increment in PL in the study species belonging to Hie two ecological groups. Mean PL in cm.

Prey length Species x ratio increment Terrestrial— Microhyla rubra 0.30 Uperodon systoma 0.32 1.07 6.25 Microhyla omata 0.35 1.09 8.57 Tomoptema rolandae 0.53 1.51 33.96

Aquatic/Semi-aquatic— Rana cyanophlyctis 0.85 Rana crassa 1.04 1.22 18.27 Rana hexadactyla 1.54 1.48 32.47 its sympatrics (i.e., with no overlaps in foraging microhabitats; see Microhabitat utilization, below). These procedures were carried out to remove effects that may mask relationships in prey use between syntopic species, such as the utilization of prey of similar dimensions in different microhabitats. Species were ranked according to the mean prey size ingested, and not according to body size. Plutchinsonian Ratios of prey length for the terrestrial frogs yielded the figures 1.1-1.5 (mean 1.2), with percentage increments of 6.3-34.0 (mean 16.3%), while values for the aquatic/semi-aquatic frogs were 1.2-1.5 (mean 1.6), with increments of 18.3-32.5 (mean 25.4%). The overall average ratio for the two groups is 1.27, with an increment of 19.9%, the mean ratio surprisingly close to 1.3, as predicted by Hutchinson (1959) for ratios of linear dimensions of the trophic apparatus in closely-related sympatric species. The data gener­ ally show lower ratios among small prey eaters, with an almost regular incre­ ment in prey length. Ratios for the linear body dimensions in the study species have been calcu­ lated by Das (1995), the mean value for HW being 1.37, when species are ar­ ranged according to body size. However, no apparent pattern of increment in the increase in PL between adjacent species could be detected, presumably because of the tendency of Uperodon systoma to take prey much smaller than expected for its head width and of Microhyla omata to ingest relatively large prey.

Prey type utilization. Based on feeding patterns, two groups of frogs are evi­ dent; a group of small terrestrial species (including Microhyla omata, M, rubra and Uperodon systoma), where a few prey categories comprise all or a major part of the diet, and a group of medium to large terrestrial or aquatic species (including Tomoptema rolandae, Polypedates maculatus, Rana cyanophlyctis, R. crassa and R. hexadactyla) that take a wide variety of prey. Included in the first group is Microhyla omata, whose entire diet comprises formicids, isopterans, coleopterans and insect larvae, and M. rubra, which takes only coleopterans and formicids. In Uperodon systoma, isopterans and formicids comprise 75% of the diet, in frequency of occurrence. Interestingly, both these otherwise quite dissimilar prey have a common gross morphology (including

1 0 J. South Asian nat. Hist. R eso u r c e u s e a n d fo r a g in g ta ctics in so u th In d ia n a m ph ibia n s

small size) and show somewhat similar spatial (clumped) distribution. Com­ pared to its sympatrics, U. systoma feeds in a remarkably sedentary fashion. All examples included in the study were collected as they foraged on the sur­ face of or close to termitaria, generally under dense vegetation during wet monsoon nights. The species does not forage anywhere else as no specimen could be found in any other microhabitat. In addition, Dutta and Pradhan (1985) noted that this frog species feeds only during rains (presumably when worker or winged termites emerge). Specimens taken by these workers at other times of the year had empty stomachs. Isopterans are taken infrequently by Rana crassa (only 1.4% of the stom­ achs examined contained this food item), whose primary food is composed of coleopterans (36.1%), insect larvae (8.3%), formicids (6.9%) and crustaceans (6.9%). Prey ingested include both aquatic (e.g., fish, tadpoles, eggs, as well as larvae of aquatic insects and aquatic hemipterans) and terrestrial (e.g., formicids, ortihopterans, blattids and chilopodans) items. Freshwater crusta­ ceans (crabs) are either taken from water during the day or from pond edges, where they wander after dark. Folivory in adult Rana hexadactyla sets it ecologically apart from its seven sympatrics at the study site, although some plant matter is occasionally in­ gested by the closely-related R. cyanophlyctis. However, a great variety of in­ vertebrate and a few vertebrate prey types are also ingested by R. hexadactyla, principally molluscs (10.3%, by frequency of occurrence) and coleopterans (8.9%). Coleopterans (26.5%, by frequency of occurrence) and insect larvae (17.7%) are the most important items in the diet of Rana cyanophlyctis, although a number of other aquatic (including molluscs, hemipterans, fish and tadpoles) and terrestrial (formicids, dipterans, blattids and orthopterans) prey are also taken. Aquatic plants (Ceratophyllum demersum) occurred in 7.8% of the stom­ achs, and constituted 10.6%, by volume, of the food biomass. The two most important items in the diet of Tomoptema rolandae, each con­ stituting 24.3% by frequency of occurrence, are formicids and coleopterans. Also ingested are insect larvae (12.9%), isopterans (8 .6%) and arachnids (7.1%). The stomachs of this species contained a large amount of dried plant and inor­ ganic debris, presumably ingested accidentally when taking small prey with its comparatively wide mouth. Of the 18 prey types identified, arthropods comprise between 6.4 (in Rana hexadactyla) and 100% in terms of total volume (in the three species belonging to the terrestrial group) of the diet. Coleopterans are primary to tertiary prey of all species, being the most commonly-occurring prey (in terms of frequency of occurrence) in as many as six of the eight species, comprising 11.1-42.9 (mean 28.1%) of the diet. While no other prey type approaches coleopterans closely in terms of occurrence in stomach samples, formicids (0-37.5; mean 15.9%), plants (0-57; mean 8.1%) and insect larvae (0-17.7; mean 7.2%) are the next most utilized groups of prey Vertebrates are only occasionally ingested but may be important in the diet of several species, and in terms of total volume, comprise 34.2% (in Rana cyanophlyctis), 2.8% (in R. crassa) and 13.1% (in R. hexadactyla). Only one fish was taken by R. crassa (1.4%), three by R. cyanophlyctis (23.3%), and 31 (9.5%)

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Table 4. Estimates of prey diversity, using the Brillouin Index (HB), based on the frequency of occurrence of prey types and dominance (reciprocal form of the Berger-Parker Diver­ sity Index (1/d), based on both the frequency of occurrence of prey types (FO) and prey size categories (PS) in the eight anuran species. Mean head width (x HW) in cm.

Species xHW HB 1/d (FO) 1/d (PS) Microhyla ornata 0.41 0.962 1.835 1.143 Microhyla rubra 0.72 0.503 1.200 1.105 Uperodon systoma 1.24 0.878 1.605 1.157 Tomopterna rolandae 1.09 1.838 3.610 1.739 Polypedates macidatus 2.09 1.069 2.500 5.000 Rana cyanophlyctis 1.61 1.952 4.016 4.098 Rana crassa 2.29 1.976 1.927 5.376 Rana hexadactyla 3.34 2.268 2.564 5.000 by R. hexadactyla. Frogs are eaten even less frequently, only one R. crassa con­ taining this item (1.4%), while R. hexadactyla contained three (3.6%) frogs. Tad­ poles are taken almost as rarely, four taken by R. cyanophlyctis (11%) and just one by R. hexadactyla (0.01%). A juvenile of the last-mentioned species had apparently fed on fish excreta (0.01%), the comparatively great volume of the items (0.05 ml) suggesting that it was not taken incidentally. Only one reptile was found: a juvenile Hemidactyhis fi'enatus (total body length, 63.0 mm) in a Polypedates maculatus (SVL 72.1 mm), which represented 31.7% of its diet by volume.

Niche breadth and overlap. Prey diversity was estimated using the Brillouin Index (HB). The results (Table 4, see also Fig. 4a) indicate a linear relationship, with a positive correlation between HW and HB (r=0.701), the scatter exten­ sive. Several small to medium-sized species (including Microhyla ornata, Uperodon systoma and Polypedates maculatus) show low dietary diversity, in­ gesting relatively few categories of prey. Larger frogs, on the other hand, tend to have wider dietary spectrum (and thus broader food niches). The weak correlation is explicable from the observation that some species take more prey items but of fewer kinds, such as small prey that show clumped distribution (e.g., Uperodon systoma and perhaps also Microhyla rubra) or one to two rela­ tively large prey (Polypedates maculatus). All four data sets were used to compute dietary overlaps, including total volume of items in each resource state (TI), frequency of occurrence of a prey resource state (FO), total volume of each resource state (TVOL) and prey size categories (PS), based on dietary data obtained from stomach analysis. Data on overlap in diet are in Tables 5-8, with a summary on Table 9. When high overlaps (O/'/c > 0.600) between species-pairs were compared (Table 11), the least number of pairs with high overlaps were found in compu­ tations for TI (16), considerably larger than for PL (18), TVOL (20) and FO (22). However, using TVOL, 3 species (Uperodon systoma, Rana cyanophlyctis and R. hexadactyla) could be clearly separated from their sympatrics as well as from one another, the low overlaps being due to food specialization in U. systoma (small insects) and R. hexadactyla (plants), whereas the dietary generalist (see Dietary Dominance, below) R. cyanophlyctis takes a wide range of prey types, and as a result shows low overlaps with its sympatrics. The relatively large

1 2 J. South Asian nat. Hist. R eso u rce u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s

Table 5. Overlap (Oyfc) in prey use (prey length) among the eight amir an species. Abbre­ viations as in Table 1.

Mo Mr Tr Us' Rc Pm Rcr Rh

Mo _ 0.999 0.194 0.999 0.131 0.063 0.125 0.160 Mr - 0.208 0.999 0.398 0.024 0.134 0.169 Tr - 0.194 0.837 0.457 0.675 0.783 Us - 0.139 0.0006 0.161 0.167 Rc - 0.416 0.822 0.929 Pm - 0.395 0.398 Rcr - 0.697 Rh -

Table 6. Dietary overlap (Ojfc) in prey use (frequency of occurrence-of each resource state) among the eight anuran species. Abbreviations as in Table 1.

Mo Mr Tr Us Rc Pm Rcr Rh Mo 0.856 0.870 0.558 0.743 0.182 0.858 0.157 Mr - 0.832 0.537 0.663 0.187 0.836 0.142 Tr - 0.734 0.779 0.350 0.811 0.170 Us ~ 0.322 0.244 0.399 0.080 Rc - 0.551 0.891 0.419 Pm - 0.499 0.163 Rcr - 0.204 Rh

Table 7. Overlap (Oy/c) in prey use (total number of prey items in each resource state) among the eight anuran species. Abbreviations as in Table 1.

Mo Mr Tr Us Rc Pm Rcr Rh Mo 0.479 0.846 0.296 0.704 0.374 0.931 0.314 Mr - 0.705 0.500 0.295 0.080 0.272 0.076 Tr - 0.710 0.637 0.337 0.694 0.259 Us - 0.099 0.009 0.070 0.012 Rc - 0.677 0.793 0.541 Pm - 0.488 0.231 Rcr - 0.348 Rh -

Table 8. Overlap (O/fc) in prey use (total volume in each prey resource state) among the eight anuran species. Abbreviations as in Table 1.

Mo Mr Tr Us Rc Pm Rcr Rh Mo 0.844 0.900 0.398 0.411 0.615 0.755 0.025 Mr - 0.901 0.196 0.369 0.684 0.830 0.016 Tr - 0.194' 0.481 0.722 0.883 0.029 Us - 0.054 0.064 0.079 0.002 Rc - 0.336 0.459 0.391 Pm - 0.736 0.015 Rcr - 0.210 Rh -

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Table 9. Summary of dietary overlap (Ojfc) in prey use (prey length, total items, frequency of occurrence and total volume) among the eight anuran species, based on data in Tables 5-8.

Overlap Type N range (x ± SE) Prey length 28 0.0006 - 0.999 (0.4169 ± 0.0638) Total items 28 0.0090 - 0.931 (0.4206 ± 0.0512) Frequency of occurrence 28 0.0800 - 0.891 (0.5013 ± 0.0534) Total volume 28 0.0020 - 0.901 (0.4142 ± 0.0607)

Table 10. Total number of high dietary overlaps (Oyfc = >0.600) in pair-wise comparisons in the eight anuran species.

Species PL TI FO TVOL Microhyla omata 2 3 4 4 Microhyla rubra 2 1 4 4 Uperodon systoma 2 1 1 0 Tomopterna rolandae 3 3 5 4 Rana cyanophlyctis 3 4 4 0 Polypedates maculatus 0 1 0 4 Rana crassa 3 3 4 4 Rana hexadactyla 3 0 0 0 Total 18 16 22 20

Table 11. Data on food volumes and the occurrence of empty gastrointestinal tracts in the eight anuran species. Abbreviations as in Table 1.

Food volumes Gastrointestinal tracts Species N Range (x.±SE) Empty % Mo 4 0.05 - 0.10 (0.063 ± 0.0125) 0 0 Mr 6 0.05 - 0.10 (0.075 ± 0.0112) 1 14.29 Us 4 0.05 - 0.70 (0.237 ± 0.155) 0 0 Tr 27 0.05 - 3.45 (0.359 ± 0.128) 9 25.0 Pm 8 0.05 - 2.00 (0.584 ± 0.272) 4 33.33 Rc 70 0.01 - 3.00 (0.340 ± 0.065) 12 14.63 Rcr 41 0.05 - 5.05 (1.015 ± 0.211) 8 16.33 Rh 206 0.05 - 18.5 (2.491 ± 0.235) 37 15.23

Table 12. Estimates of microhabitat niche breadth, using the Shannon-Weiner Index (HO and dominance, using the reciprocal form of the Berger-Parker Index of Diversity (1/d) in the eight anuran species.

species H' 1/d Microhyla ornata 0 1 Microhyla rubra 0.377 1.143 Tomopterna rolandae 0 1 Uperodon systoma 0 1 Rana cyanophlyctis 0.464 1.212 Polypedates macidatus 0.303 1.100 Rana crassa 0.911 1.626 Rana hexadactyla 0.572 1.350

14 ]. South Asian nat. Hist. R eso u rc e u se a n d fo r a g in g ta ctics in so u t h In d ia n a m ph ib ia n s

Table 13. Microhabitat overlap (Oy/c) among the eight anuran species. Abbreviations as in Table 1.

Mo Mr Tr Us Rc Pm Rcr Rh Mo - 0.141 0 0 0 0 0 0 Mr - 0.999 0 0 0 0 0 Tr - 0 0 0 0 0 Us - 0 0 0 0 Rc - 0 0.926 0.069 Pm - 0 0 Rcr - 0.419 Rh -

x H W

Figure 4. (a) Relationships between mean head width and the BriHottin Index of Diver­ sity; (b) mean head width and the Berger-Parker Index of Diversity based on frequency of prey resource use; and (c) prey size-category frequency, in the eight anuran species.

Vol. 2., No. 1. 15 number of species that show high overlaps with R. hexadactyla when (animal) PL is used is because plant matter, the most-important dietary constituent of this species, is ignored, and thus the overlap values may be grossly exagger­ ated. Within ecological groups (i.e., aquatic/semiaquatic species versus terres­ trial ones), overlap values did not differ significantly for any of the three meas­ ures (f-test, £=-5.946-0.538, d.f ~2, P > 0.05). When overlaps for FO were regressed with overlaps for TI, PL and TVOL (Figs. 5a-5c), more biologically significant trends were noticeable. For the FO-TI relationship (Fig. 5a), the correlation indicates a positive association

OVERLAP FO

OVERLAP FO

OVERLAP FO Figure 5. Relationships between measures of dietary niche overlap: (a) frequency of occurrence and total number of items; (b) frequency of occurrence and prey length; and (c) frequency of occurrence and total volume, in the eight anuran species.

16 J. South Asian nat. Hist. R eso u rc e u s e a n d fo r a g in g ta ctics in so u th In d ia n a m ph ibia n s

(1=0.783)/ as do the relationship between FO and TVOL (r=0.665; Fig. 5c). Thus species-pairs maybe considered basically similar in their usage of prey resources, whether the comparison is by FO or TI. However, there appears to be no corre­ lation (r=0.241) between FO and PL overlaps (Fig. 5b). This may reflect the fact that size, rather than prey type, is important in prey selection in this frog com­ munity. Similar trends have been noticed by Schoener (1968) from sympatric anoline lizards in central America, and may be generally true of predators that ingest their prey whole, especially insectivores.

Dietary dominance. To examine the relationship between dominance of food items (frequency of occurrence) and size or life history of the frogs in the study area, the Berger-Parker Diversity Index was employed. The results (the recipro­ cal form of the index, 1/d, used to ensure that the index increases with increas­ ing diversity) have been summarized in Table 4. There appears to be no rela­ tionship between the dominance of food items and frog gape size (r=0.219; Fig. 4b). Abetween-group comparison (aquatic/semi-aquatic versus terrestrial, mi­ nus Polypedates■ maculatus; see Microhabitat utilization below, for justification) indicates no significant statistical difference between the two groups (t-test, t=- 2.396, d.f.=2, P > 0.05). The biological significance of some of these values is, however, apparent, since higher 1/d values imply the ingestion of fewer items of a single resource type, and thus indicate a dietary generalist (as opposed to food specialists, that should primarily concentrate on one or a few food types). The highest dominance was found in Rana cyanophlyctis (4.07) and Tomopterna rolandae (3.61). Rana hexadactyla, however, has a lower dominance value (2.56) than would be expected for its body size. Since 39.01% (total food items) of its ' -{j diet comprises plants, all of which have been considered a single resource state in this analysis, a recalculation of the data, with plant resources divided further into high LPI gives a Diversity Index value (1/d) of 6.80 and a stronger correla­ tion between HW and the Diversity Index of the study species can be obtained (r=0.718). Dominance was also calculated for prey size use to determine relative utili­ zation of prey size-classes by the eight sympatric frog species. Results (summa­ rized in Table 4) show a fairly constrained relationship of mean HW to domi­ nance (r=0.867; Fig. 4c), larger frogs ingesting a wider prey size range than smaller ones, as already indicated by the relatively higher cv values in the larger spe­ cies, compared to their smaller sympatrics (see Size relationship with prey, above). To summarize, larger frogs tend to have lower dominance, or higher even­ ness in diet, and tend to be generalists in terms of prey size selected, while smaller species are, without exception, dietary specialists.

Prey numbers and food volume. Smaller frogs tend to eat more individual ani­ mal prey (although not more in terms of volume) than larger ones (Table 1), with prey numbers differing significantly between species (one-way ANOVA, P7/245=30.70, P < 0.001). The relationship between mean HW and mean number of prey items (Fig. 6.1) is significant (P < 0.05) and positive (r=0.778), although still with considerable scatter, since several species take more (e.g., Uperodon systoma, which takes 11-235, mean 95.2 tiny prey) or less (e.g., Polypedates maculatus, that eats only 1-2, mean 1.2 large prey) items than expected from the dimension of the trophic apparatus.

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Food volume, which varied significantly between species (one-way ANOVA, F7f35Q=7.73, P < 0.001) is expected to show a positive relationship with body size, since larger frogs should be able to ingest more food than smaller ones. The relationships between mean HW and food volume (Fig. 6 .2) on log- log paper, based on data in Table 10 shows a highly positive correlation (r=0.958), the slope (b) being -0.69, significantly (Mest, P < 0.05) less than needed for isometry for regression of linear dimension to volume, the correla­ tion significant (P < 0.05). These findings reveal'that larger frogs eat more food than smaller ones, although increase in food intake with increasing gape size (here HW) is disproportionately small. The number (and percentage) of empty gastrointestinal tracts (Table 10) is instructive in understanding feeding patterns, especially foraging success. The percentage of empty tracts (all examined within three hours of capture) ranged between 0 m b oih Microhyla ornata and Uperodon systoma (both small-prey eat­ ers) to 33.33 in Polypedates maculatus (a large-prey eater), with their sympatrics showing intermediate values. Small-prey eaters therefore not only harvest more prey (Table l)/but also have higher foraging success (Table 10) than do large-prey eaters. Species that eat larger (and presumably more nutritious) meals can, ac­ cording to the optimal foraging theory, afford to bypass many inferior (usu­ ally small) prey, thereby selectively foraging on large prey which may imply fewer meals per unit time compared to the small-prey eaters. Polypedates maculatus selects extremely large prey that occasionally approach the predator in body size and appears to ignore many small prey items that are ingested by its sympatrics. Small predators (or members of the terrestrial group), which are consid­ ered to display the WF mode, take smaller prey than larger ones (the aquatic/ semi-aquatic group, as well as Polypedates maculatus), but in greater numbers (Fig. 7; data from Table 1). Active foraging is presumably energetically expen-

logS HW logxH W

Figure 6. (a) Relationships between mean head width and mean animal prey eaten, and (b) mean head width and mean food volume, in the eight anuran species.

18 J. South Asian nat. Hist. R e so u r c e u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s

logx prey length Figure 7. Relationship between mean prey length and mean prey items in the eight anuran species, on a log scale. sive, and a WF predator should catch more prey per unit time than a SW one (Huey and Pianka, 1981; Toft, 1981). Cluster analyses based on the dietary overlap data reveal close associa­ tions within the small prey eaters (including Microhyla ornata, M. rubra and Uperodon systoma), which together form a tight and highly conspicuous guild (Figs. 8 and 9), when prey number and prey length are considered. The op­ portunistic and sit-and-wait insectivores (including Tomopterna rolandae, Rana cyanophlyctis and R. crassa), plus the sole folivore (R. hexadactyla) together form a less tightly-clustered group (Figs. 8 and 9), while the energy-maximizer (Polypedates maculatus) falls out clearly from this second group in the clusters of both prey volume and prey length. In terms of total volume of prey harvested (Fig. 10), the pattern of associa­ tion appears less well defined, with Rana crassa only slightly apart from Microhyla ornata and M. rubra, which join Tomopterna rolandae in a close cluster. However, Uperodon systoma, a small prey specialist, is clearly far apart from its phylogenetically close relatives M. ornata and M. rubra (all belonging to the family Microhylidae), to which it is ecologically close on the basis of prey num­ bers and prey size harvested. When frequency of occurrence is considered (Fig. 11); species associations are even less obvious: Microhyla ornata and M. rubra are still close, although most species are rather loosely associated. The relatively tight clustering of species when prey length and prey numbers are considered appear to be re­ flective of both prey size and prey behaviour (e.g., prey gregariousness, as in the case of ants and termites), suggesting that prey size is more important to frogs than prey resource types. Microhabitat utilization Much of the current concept about microhabitat use by amphibians, as well as methodologies used in its study, is derived from the work of Inger and Colwell (1977). Although fairly coarse divisions of microhabitat resource states were made in the present study, separation of the eight species is evident. Based on observations of undisturbed, and presumably foraging, individu­ als of the eight species of anurans at the study site, eight microhabitats were recognised: microhabitat 1; on the surface, in paddyfields and Casuarina for-

Vol. 2., No. 1. 19 DAS

Microhyla omala Microhyla rubra Uperodon systoma Tomopterna rolandae - Rana hexadactyla - Rana cyanophlyctis - Rana crassa - Polpedates maculatus------'

Prey number overlap

Figure 8. Cluster analysis of data on prey number overlaps between the eight anuran species.

Microhyla ornata -j Microhyla rubra -I Uperodon systoma J Tomopterna rolandae------Rana hexadactyla------Rana cyanophlyctis------Rana crassa______Polpedates macidatus------' Prey length overlap

Figure 9. Cluster analysis of data on prey length overlaps between the eight anuran species.

Microhyla ornata Tomo'ptema rolandae ■ Microhyla rubra ■ Ranaci'assa ■ Polpedates macidatus ■ Rana cyanophlyctis ■ Rana hexadactyla • Uperodon systoma ■ Prey total volume overlap

Figure 10. Cluster analysis of data on prey volume overlaps between the eight anuran species.

Microhyla ornata • Microhyla rubra ■ Tomopterna rolandae • Rana crassa ■ Rana cyanophlyctis ■ Uperodon systoma ■ Polpedates maculatus ■ Rana hexadactyla ■ Frequency of occurrence of prey type overlap

Figure 11. Cluster analysis of data on frequency of occurrence of prey resource states overlaps between the eight anuran species.

2 0 J. South Asian nat. Hist. R eso u rc e u se a n d fo r a g in g ta ctics in so u th In d ia n a m ph ibia n s

Microhyla ornata ------Tomopterna rolandae ------>______Microhyla rubra - ' ______Uperodon systoma ------Polpedates macidatus ------1_____ Rana hexadactyla ------i j Rana crassa — i______Rana cyanophlyctis — ' Microhabitat overlap Figure 12. Cluster analysis of data on microhabitat overlaps between the eight anuran species. ests; microhabitat 2; edges (< 0.5 m depth) of permanent or ephemeral waterbodies; microhabitat 3; deeper (> 0.5 m depth) parts of permanent waterbodies; microhabitat 4; banks of permanent or ephemeral waterbodies; microhabitat 5; ephemeral waterbodies; microhabitat 6; vicinity of termitaria; microhabitat 7; on trees; and microhabitat 8, vicinity of human dwellings. As with dietary niche breadth, microhabitat breadth (measured using the Shannon-Weiner Index) generally increased with frog size (Table 12), imply­ ing a greater plasticity in microhabitat usage by the larger frog species. This tendency is also noticeable in the dominance (1/d) values, larger species show­ ing higher dominance (or lower evenness) compared to the smaller ones. These patterns may result, in part, from shifts in habitat usage during ontogeny in some species (see below), and also the ability of some species to utilize more than a single microhabitat type. For instance, Rana cyanophlyctis is able to exist in two different microhabitats (ephemeral and permanent waterbodies) in two colour morphs (the polymorphism thought necessary to achieve this has been discussed by Das, 1992) and Polypedates maculatus is able to forage both on the surface and in arboreal situations. Microhabitat overlaps were estimated using the symmetric (fide Pianka, 1986) version of the MacArthur and Levins' (1967) formula. Mean overlaps (Ojk) between species were generally low (0-0.999, mean 0.091 ± SE 0.049), significantly (£-test, P < 0.0001) lower than dietary overlaps using prey size, total items, frequency of occurrence or total volume. Microhabitats of sympatric species at the study site are thus widely separated, with two species (Polypedates maculatus and Uperodon systoma) showing no overlap when paired with their sympatrics. In terms of microhabitat sharing, Rana cyanophlyctis overlapped broadly with R. crassa (0/7c=0.926), but substantially less with the closely-re­ lated R. hexadactyla (0/7c=0.069), both R. crassa and R. hexadactyla themselves overlapping only moderately. The Microhyla ornata-M. rubra pair overlapped only weakly (0/7c=0.141), M. rubra associating with Tomopterna rolandae much more frequently (0/7c=0.999). The low mean overlap values suggest that the species constituting the community are less tightly packed, as Inger and Colwell (1977) discovered among amphibians and reptiles from agricultural ecosys­ tems, with closely-related species showing less overlap in microhabitat usage with each other than with other species. The cluster showing the microhabitat associations between the eight syntopic anuran species (Fig. 12) shows little evidence of guilds. At best,

Vol. 2., No. 1. 2 1 Microhyla ornata, M. rubra and Tomopterna rolandae can be described as rather loosely-associated, as are Uperodon systoma, Polypedates maculatus and Rana hexadactyla. R. crassa and R. cyanophlyctis seem the closest, both inhabitants of pools of various types within the study area. Inger et al. (1987) found ontogenetic shifts in microhabitat used by two of three anurans they studied. In this study, overlaps (Ojk) between the early pre-metamorphic stages (SVL < 4.26 cm) and adults (SVL > 4.26 cm) of Rana hexadactyla was 0, indicating no similarity in microhabitat usage. Metamorphs of R. hexadactyla are confined to the edges of permanent waterbodies, while adults utilize deeper waters. This separation is probably due to biophysical factors (small frogs probably cannot be totally aquatic, being too heavy rela­ tive to body size). The separation of microhabitats between the early and late post-metamorphic stages of R. crassa was, however, less dramatic, the overlap (Ojk) being 0.46. Adults of this species utilize edges of ephemeral waterbodies along with the juveniles, in addition to occurring in deeper waters. Activity p attern Inger and Colwell (1977) discovered that anuran amphibians do not lend them­ selves easily to (diel) temporal separation. All species in the study site are largely nocturnal, although the SW ones fed opportunistically during the day too. However, some seasonality in activity patterns within the community is evident, and the following section discusses some qualitative results and im­ pressions on the use of temporal resources by the study species. Of the eight species, five (or 62.5%) are nocturnal terrestrial and/or arboreal (including Microhyla ornata, M. rubra, Uperodon systoma, Tomopterna rolandae and Polypedates maculatus). Among these, only P. maculatus utilizes trees. The remain­ ing three species, or 37.5% (Rana cyanophlyctis, R. crassa and R. hexadactyla) are largely nocturnal and aquatic/semi-aquatic. No species at the study site are diur­ nal and terrestrial, only the aquatic R. cyanophlyctis and R. crassa being partially diurnal. The absence of diurnal and terrestrial frog species may be due to physi­ ological constraints, reduced prey availability or increased diurnal predation, or possibly an interaction of more than one factor in concert. Optimal foraging theory predicts that diets should contract in terms of di­ versity during the resource-abundant season, and expand during the "lean" one, and to maximize returns, a predator has to capture prey that provides more energy than invested in their pursuit and capture. Judging from the observations on twb of the three non-SW species (Microhyla rubra and Uperodon systoma), activity is restricted to the wet season. Possibly low returns per unit of foraging time invested render them unable to operate during the dry sea­ son, although it is possible that their inactivity may.be due to physiological constraints, such as increased water loss. Uperodon systoma, in particular, dem­ onstrates this effect well, its emergence being timed to the swarming of ter­ mites on the surface during rainy nights. Toft (1985), in her review of resource partitioning, found that time, either diel or seasonal, is partitioned secondary to the partitioning of food or microhabitat in frogs, and concluded that temporal partitioning, by itself, may not be very important. Implicit from the findings of this study is the presence of seasonality in activity within some species in the community that feed se­ lectively on a few types of prey.

2 2 J. South Asian nat. Hist. R e so u rc e u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s

Discussion The ways in which predatory species forage have long been of interest to ecolo­ gists, and on the basis of the manner by which it is accomplished, two basic modes may be employed: sit-and-wait predators are largely sedentary, relying on prey density and mobility, whereas widely-foraging ones actively search for often less mobile prey, relying on the spatial distribution of prey and their own capabilities to search for them (Pianka, 1966). Widely-foraging species, such as Microhyla ornata and M. rubra, which show narrow diets (see Niche breadth and overlap, above) and warning colouration (Das, 1992) maybe con­ sidered 'pure pursuers7 (sensu MacArthur and Levins, 1964). Such predators are expected to have a search image for small prey (but see Guilford and Dawkins, 1987, for an alternative viewpoint), stereotyped search behaviour and possibly exclusive use of an established foraging area. Sit-and-wait spe­ cies (in this study, Rana cyanophlyctis, R. crassa, R. hexadactyla, Polypedates maculatus and Tomopterna rolandae), on the other hand, appear to locate prey by scrutinizing a foraging area, and show a greater range of both food types and prey sizes, compared to the non sit-and-wait types. True widely-foraging species in the study area include only Microhyla ornata and M. rubra, together comprising 25% of the community in terms of num­ bers. The foraging strategy of Uperodon systoma seems fundamentally differ­ ent from that of its closest relatives. Huey and Pianka (1981) argued that ter­ mites are more likely to be the food of widely-foraging species than of sit-and- wait ones. Uperodon were only found on rainy nights at the height of the Southwest Monsoons (July 10, and August 4 and 5), and all specimens were taken from or close to termitaria, where the frogs were observed feeding on worker termites. The prey of the southwest African lizards studied by Huey and Pianka (1981) were harvester termites (.Hodotermes sp.) which are known to undertake periodic foraging expeditions (Bouillon, 1970), unlike the mound- building termites in the present study. The foraging modes of the two groups of termites are thus quite different. In addition, if the nature of foraging by the prey species influences predator foraging behaviour, it is not always in pre­ dictable ways. Krebs (1978) generalized that the food of sit-and-wait preda­ tors should be widely-foraging prey, while widely-foraging predators should harvest sit-and-wait prey Harvesting termites are widely-foraging and are eaten by lizards exhibiting the same foraging mode according to the data in Huey and Pianka (1981). Mound-building termites that have restricted motil­ ity during foraging are preyed upon by Uperodon, which emerge seasonally during the rains to feed on the generally subterranean termites, and thus these largely fossorial frogs do not appear to show either end of the sit-and-wait- widely-foraging continuum, suggesting that foraging modes may be more complex than sometimes assumed- The strategy of feeding on prey such as termites which show clumped dis­ tribution and are seasonally available, is presumably both energetically inex­ pensive and reduces the chance of predation. However, it may demand crypsis, as in predators of the sit-and-wait mode. The feeding strategy of Uperodon may be termed "sit-and-eat" instead, and may have evolved from a widely- foraging mode, resulting in a more specialized morphology and the return of the cryptic colouration scheme displayed by the generalized anuran forms.

Vol. 2., No. 1. 23 DAS

The high use of certain food items by several species is remarkable. If those taxa taking over 60% of a single category of food are considered dietary spe­ cialists, Microhyla rubra (formicids, 66.1% by volume), Uperodon systoma (isopterans, 68.4%) and Rana hexadactyla (plants, 79.3%) emerge as dietary spe­ cialists. The number of prey resource states used by the eight sympatric spe­ cies varied greatly, and on the basis of the various types of prey utilized, four groups of frogs could be identified: 1. Terrestrial small-prey eaters (including Microhyla ornata, M. rubra and Uperodon systoma), that fed on 2-5 (mean 3.67) prey types. 2. Terrestrial large-prey eater (Polypedates maculatus), that took 6 resource types. 3. Terrestrial dietary generalist (Tomopterna rolandae), which ingested 10 prey types. 4. Aquatic and semi-aquatic small to large prey-eaters (including Rana cyanophlyctis, R. crassa and R. hexadactyla), which took 15-19 (mean 16.33) categories of prey. Frogs belonging to group 1 are considered to be widely-foraging (Pianka, 1966), with the exception of Uperodon systoma ingesting a narrow prey spectrum that probably need to be located by actively searching on the ground. Group 4 includes sit-and-wait frogs that show a wide prey diversity and are thought to feed opportunistically on largely mobile prey, although some stationary (in­ cluding aquatic insect larvae and plants) and slow-moving (molluscs) prey are also taken. In between these two ends of the continuum two more catego­ ries can be added, including group 3 (Tomopterna rolandae), considered a di­ etary generalist, that takes both small and spatially clumped (e.g., isopterans), and medium to large and randomly-distributed (most other items taken) prey resources. Also included within this continuum is the group 2 predator, Polypedates maculatus, which appears to forage selectively and probably opportunistically on large prey. Although this species shows a diet almost as narrow as the widely-foraging species (group 1), it hunts by ambush (i.e., sit- and-wait), the mode of foraging and the nature of prey probably account for the low success in capturing prey, as evident from the large number of empty stomachs (see Prey numbers and food volume, above). Since frogs swallow their prey whole, the head width at the angle of the jaws is a good indicator of gape, and may thus provide an estimate of the prey size taken by each species. When the eight anuran species in the study com­ munity are arranged in a size-series, a mean ratio of 1.37 (range 1.10-1.76) be­ tween consecutive pairs of frogs is obtained. Hespenheide (1975) stated that among insectivorous species, prey size selected is correlated with the size of organ used in prey capture. This generalization may perhaps be regarded as somewhat simplistic, since species constituting real communities may show adaptive variations that appear contrary to the above. Within the community studied, the larger species tend to show greater ranges of variation in prey length than smaller ones. Selective foragers (i.e., the widely-foraging species) which specialize on small prey have lower coefficients of variation of prey length than the non-discriminant ones (sit-and-wait species). In general, prey size correlates more strongly with gape in small-prey eaters than in the species that could take large prey, which, presumably because of a wider gape, could consume a wider size-range of prey.

24 J. South Asian nat. Hist. R eso u r c e u s e a n d fo r a g in g ta ctics in so u th In d ia n a m ph ibia n s

Apparently to compensate for harvesting small prey, widely-foraging frogs take more prey items per unit time than sit-and-wait ones, as there is a nega­ tive correlation between mean prey size and mean prey number when all spe­ cies are compared. Active foragers are thought to expend more energy per unit time and thus may be required to harvest more prey than sedentary for­ agers, which depend more on prey abundance and mobility than their own searching abilities (Pianka, 1986). At one extreme of the sit-and-wait mode is Polypedates maculatus, which tends to eat large prey, while apparently bypass­ ing smaller ones. Mean prey length (3.13 cm) in this species is significantly greater than those taken by its sympatrics, the selective foraging probably being a result of utilization of microhabitats which no other members of the community can exploit, with overlaps in the foraging places with other spe­ cies being zero. The strategy of feeding selectively on large prey should help optimize energy returns, according to Schoener's (1971) foraging theory. Smaller species in the study area are considered to be more specialized, which is in accordance with the beliefs of Hutchinson (1959) and Schoener (1986), since smaller species tend to show both narrower food and microhabitat niches, relative to their larger sympatrics. All species at the study site feed during the wet season. Two (.Microhyla rubra and Uperodon systoma) of the three non sit-and-wait species become inac­ tive during the dry periods, possibly because active foraging (e.g., M. rubra) during the Tean resource7 season is energetically expensive, physiologically difficult on account of moisture loss and because of the non-availability of certain prey types, such as termites (the primary food of U. systoma). The sit- and-wait mode is thought to be a more effficient foraging strategy during the dry period at this study site, net gains per unit energy spent being higher than for active foraging (see Huey and Pianka, 1981). In addition, all sit-and-wait frogs operate in or at the edge of water bodies, and therefore are not constrained by moisture loss. Larger species within the community tend to show wider trophic niches, compared to smaller species, although this trend is somewhat obscured by some species of intermediate body size that appeared to have evolved food specialization for a few prey resource types (and hence have narrower food niches). Food niches, in general, increase with increasing body size in preda­ tors, since larger predators can take a wider size range of prey (Pianka, 1988). Increases in dietary niches with ontogeny in salamanders and frogs have also been discovered by Kuzmin (1990). However, an exception is on record: Barclay and Brigham (1991) showed that the above generalization does not hold for chiropterans that feed on flying insects, since the prey detection system of large bats is unable to detect small prey Invertebrates, especially arthropods, are the most important category of prey for the species of the community under study, in terms of frequency of occurrence, total volume, or total items in stomach samples. However, verte­ brate prey, including fishes, frogs, tadpoles and lizards are taken by four (.Polypedates maculatus, R. cyanophlyctis, R. crassa and R. hexadactyla) of the eight species, and in terms of volume, may be important dietary constituents. Verte­ brates are ingested in larger quantities by pre-reproductive adult females of R. hexadactyla. This is considered a response to increased seasonal metabolic re­ quirements associated with the production of reproductive tissue (Das, 1996).

Vol. 2., No. 1. 25 DAS

For metamorphosed R. cyanophlyctis, conspecific tadpoles formed 11% of the total diet by volume, this prey resource state being taken both during the be­ ginning (February and September) and end (June) of the dry seasons. Canni­ balism is a stabilizing factor during and after periods of food shortage in a cyclopoid predator-prey system (Gabriel, 1985). When frog species are ranked according to size, food specialists (widely- foraging frogs) were smaller, dietary generalists in between, and species that selected large prey at the other extreme of the size range. Deviations from the expected pattern are the foraging strategies of Uperodon systoma, which feeds exclusively on tiny prey showing a clumped distribution, Polypedates maculatus, which elects extremely large prey and the largely-folivorous adults of Rana hexadactyla. Among frogs at the study site, widely-foraging species are brightly-col­ oured, and at least one species (.Microhyla omata) has been shown to have a noxious secretion, while M. rubra displays a "facial pattern" on the rump that is concealed when the hind limbs are retracted (Das, 1992). These small-prey eaters have in addition a relatively narrow gape and wider eyes associated with improved vision for foraging at night. Uperodon systoma, while similar to the widely-foraging frogs in showing a relatively narrow gape and large eyes, has, unlike them, short and very thick hind limbs. Its dorsum colouration comprises a pattern of dark blotches on a pale background and is thought to be for crypsis since foraging is sedentary. An extremely well developed tarsal tubercle that acts as a cutting edge during sweeping motions of the limb while burrowing is found in all the back-first burrowing species of known amphib­ ians. None of these small-prey eaters possesses dentition, either on the max­ illa or on the prevomerine region, probably because teeth are of little use in catching or processing their prey. However, the tongue is broadened and lobeless, a feature thought to be adaptive for picking up spatially-concentrated, small prey in large numbers from the surface. Ants and termites are chitinous, low-nutrient food items (Pianka, 1981), and appear to require harvesting in large quantities. This is reflected by the extremely large stomach (mean STVOL/ SVL3 ratio 3.76), relative to body size in IT. systoma (Das, 1995a). All sit-and-wait species, on the other hand, show cryptic colouration. Some (including Rana crassa and R. hexadactyla) show polymorphism in vertebral striping or in the colour and pattern on the dorsum (e.g., R. cyanophlyctis). This is thought to reduce predator efficiency and improve utilization of different microhabitats, respectively. All species employing this foraging mode ingest a wider range of prey types and sizes than widely-foraging species, and have a comparatively wider gape, smaller eyes (since prey are caught in ambush, and not actively searched for) and short limbs. One exception is the scansorial Polypedates maculatus; the long legs of this species are clearly adaptive for climb­ ing and jumping. Since prey are frequently taken from a distance with the aid of the lingual apparatus, the tongue is generally bilobed (trilobed in the folivorous Rana hexadactyla), the lobes increasing the surface area of this sticky catapult. Tomoptema rolandae has been considered a dietary generalist, its foraging strategy at neither end of the sit-and-wait-widely-foraging continuum. The species overlapped in food with both the small-prey eaters as well as the large- prey eaters, and shows characteristics intermediate between these two groups,

26 J, South Asian nat. Hist. R eso u r c e u s e a n d fo r a g in g ta ctics in s o u t h In d ia n a m ph ibia n s such as body size and stomach volume. This species has the widest relative gape among the eight species, reflecting of the wide size range of prey in­ gested. Compared to the other aquatic/semi-aquatic species, Rana cyanophlyctis is also a dietary generalist, taking a wide prey spectrum, although aquatic coleopterans dominate its diet. There appears to be evolutionary convergence (Grinnell, 1924; see also Terborgh and Robinson, 1986, for a review of concepts) between the commu­ nity examined here and that reported by Toft (1980; 1981). In morphology and foraging tactics employed, members of the community investigated appear to parallel the New World (Peruvian and Panamanian) anuran fauna, with nar­ row-mouthed, brightly coloured species that eat relatively more ants and ter­ mites (almost all dendrobatids and a bufonid, in the New World rainforests; microhylids of the genus Microhyla in this study site), and wide-mouthed, cryp­ tic, non-ant eating sit-and-wait species (leptodactylids in the New World, most ranids and a rhacophorid in the present study), that hardly ever touch ants and termites. The findings described here support the hypothesis that ecology, (foraging) behaviour and morphology have coevolved (Williams, 1972). Feeding on prey that is probably restricted both seasonally and tempo­ rally, Uperodon systoma shares its primary food with fewer species, while the diets of its sympatrics overlap considerably more with each other. Toft (1980) compared ant and termite specialists to grazers and browsers, since only non- reproductive units (workers and soldiers) of their prey are eaten, while sit- and-wait species prey more frequently on reproductive animals. Of the total of 136 ants and 231 termites found in stomach samples of U, systoma in this study, all except a single queen ant, belong to the non-reproductive castes. Feeding is probably restricted to the soil surface on rainy nights when termites are active and accessible, since unlike vertebrate (e.g., Maras crassicaudata, which occurs in the study site) or invertebrate (perhaps ants) termitophages, this species probably is too large and lacking specialized features (e.g., claws, like mM anis) to invade the termitaria. Some feeding inside the termitaria, close to the surface, may have gone unnoticed, but this species apparently does not feed at other times of the year (Dutta and Pradhan, 1985). This concentrated food source is therefore available only seasonally and feeding bouts are re­ stricted to a short period each year. Pulliam (1974) argued that when a preda­ tor discovers such a food source, no further foraging is involved until all prey have been consumed. Since the food supply from such a source is abundant and has the potential to satiate small termitophages such as Uperodon during every feeding bout, the same termitarium may be used for a long time, possi­ bly for several seasons, by one or more individuals which may congregate on it during the 'right' time (i.e., rainy nights). • While food specialists can be clearly separated ecologically from their sympatrics, the relationship (including the potential for competition) between dietary-generalist species-pairs with high overlaps in resource use is much more complex. High overlap values are not necessarily proportionate to the intensity of competition (Pianka, 1986). In certain situations (such as a resource- abundant environment) two ecologicaHy-similar species should be able to co­ exist indefinitely with total dietary overlap (both species consuming the same resource states in the same proportion). Food competition can be demonstrated only when depletion of food resources is shown together with negative inter­

Vol. 2., No. 1. 27 DAS actions between organisms, which is known in experimental conditions, but not in nature, for amphibian communities (see Kuzmin, 1995). Similarity in diets have even been proposed as evidence for lack of food (limitation and) competition (e.g., Licht, 1986; Kuzmin and Tarkhnishvili, 1991; 1992). As no data are available to indicate whether food is limiting in the study area (which would presumably include information on the quantity of food required for frogs to both survive and spawn), the question about the role of competition between the members of the community under study remains unanswered. Hutchinsonian Ratios discovered in the members of the community under study (see Das, 1995a) is an indirect evidence for food competition. Addition­ ally, cannibalism of its tadpoles by metamorphosed Rana cyanophlyctis, which may be considered an example of interference competition (see Miller, 1967) may be the result of food limitation in the environment. The ingestion of a wide size-range of prey by the larger frogs (including Rana crassa and R. hexadactyla), and folivory in R. hexadactyla may be other effects of food scarcity in the study area. However, single factors, such as competition or predation, is no longer thought to determine the structure of communities, a growing body of evidence showing that controlling factors vary both temporally (Wiens, 1977) as well as spatially (Mittlebach, 1988). Sympatric species overlapped broadly in diet and somewhat less so in microhabitat (although the most closely-related species overlapped the least). Temporal partitioning patterns within the community were indeterminate, but species that feed selectively are distinctly seasonal in their activity patterns. Dietary niche breadths tend to increase with mean body size, especially gape, presumably because larger species can ingest food resources not available to their smaller sympatrics (including larger prey or plant matter). However, certain adaptive strategies may at least partially conceal this pattern, some species taking many prey items of a few resource types (e.g., Uperodon systoma) or a few large prey items (e.g., Polypedates maculatus). Microhabitat niche breadths also showed this pattern, and must be due to the ability of the larger species to use more than a single microhabitat type. In addition, at least two of the largest species at the study site (Rana crassa and R. hexadactyla), show shifts, partial or entire, in microhabitat types used during ontogeny. A gen­ eral conclusion is that larger species, due to a greater plasticity in their use of food, space and seasonal time tend to be generalists, compared to their smaller sympatrics. Acknowledgements This study was supported by the Inlaks Foundation, Madras Crocodile Bank Trust, Trinity College, Oxford and an Overseas Research Student (ORS) Award. For discussion and comments on the ideas presented, I thank Roger A. Avery, Malcolm J. Coe and Peter J. Miller. Romulus Whitaker provided support and facilities to conduct the field study, and for assistance in the field, I am grateful to Chockalingam. Literature cited Barclay, R. M. R. & R. M. Brigham 1991. Prey detection, dietary niche breadth, and body size in bats: Why are aerial bats so small? American Natur., 137: 693-703. Bouillon, A. 1970. Termites of the Ethiopian region. Pp. 153-280 in Krishnan, K. and F. M.

28 J. South Asian nat. Hist. R eso u r c e u se a n d fo r a g in g ta ctics in so u th In d ia n a m ph ibia n s

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30 J. South Asian nat. Hist.