The food of the Giant Toad Bufo asper MRS P. Y. BERRY

Zool. J. Linn. SOC., 49, pp. 6168. With 2 figures May 1970 The food of the Giant Toad Bufo asper MRS P. Y. BERRY School of Biological Sciences, University of Malaya, Kuala Lumpur, Malaysia Accepted for publication 19 August 1969 Examination of the stomach contents of 93 Bufo asper from Templer Park and Batu Caves, Selangor, Malaysia, shows that it feeds upon a wide range of invertebrates. Little or no marked seasonal variation in the diet was found. The relationship between predator and prey size and the interspecific variations in the diet of B. asper, B. melanostictus and other Bufo species are discussed. CONTENTS Introduction. Materials and Methods. Characteristics of collecting localities. Examination and recording of stomach contents Results Composition of the diet. Seasonal variation in food intake. Food in relation to size.. Discussion. Summary. References. INTRODUCTION PAGE... 61. 62. 62. 62. 63. 63. 64. 65. 65. 67. 68 Comparatively little work has been done in Malaysia on the food of amphibians. Serry & Bullock (1962) examined the food of Bufo melanostictus Schneider from Malaysia and Singapore and found that it fed on a wide range of ground and litterdwelling invertebrates with apparently little selectivity. Investigations on the food of amphibians collected on Pulau Tioman showed that their diet depended on the preferred feeding sites of the frogs (Bullock, 1966). Similarly, Berry (1965) found that the availability of prey largely determined the diet of Rana limnocharis Wiegmann, and Rhacophorus Zeucomystax (Gravenh.) from Singapore. On the other hand, studies on the diet of Leptobrachium na&ops Berry & Hendrickson, and three microhylid species, Kaloula pulchra Gray, Microhykz heymonsii Vogt and M. butleri Blgr., showed that they had a definite preference for a particular prey type. L. nigrops preferred larger prey such as gryllids, blattids, and spiders while the microhylids preferred small animals such as acarines, ants and termites (Berry, 1965). Likewise, Berry (1966) found that the torrent frog Amolops larutensis (Blgr.) selected prey animals within the sizerange of 106.5 mm although frogs greater than 30.0 mm from snout to vent were capable of ingesting prey larger than 16 mm length. The present investigation forms part of a survey of Malaysian amphibians living in a wide range of habitats. The species chosen, Bufo asper Gravenh. lives on the floor of 5 61 Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

62 MRS P. Y. BERRY primary forest and also in caves in limestone outcrops. B. asper is the largest member of the Bufonidae occurring in Malaya, the adults measuring more than 160 mm from snout to vent. MATERIALS AND METHODS The material in this study was collected from two localities. Fiftyfour specimens were obtained from Templer Park, Selangor, between April 1962 and April 1963, and 39 individuals were taken from Batu Caves, Selangor, in four separate collections (April, May and October 1962, and in January 1963) (Table 1). Table 1. Number and seasonal distribution of toads collected from Templer Park and Batu Caves Month Locality r 7 Templer Park Batu Caves AprilMay 1962 11 24 JuneJuly 5 AugustSeptember 3 OctoberNovember 6 7 DecemberJanuary 1963 13 8 FebruaryMarch 9 AprilMay 7 Total 54 39 Characteristics of collecting localities Templer Park is a primary rain forest reserve 1415 miles north of Kuala Lumpur, Selangor. The area is 500750 feet (152229 m) above sealevel and has many waterfalls and footpaths. The toads were collected at night along footpaths, near the edges of waterfalls, and along the banks of streams. The second locality, Batu Caves, is a series of adjoining caverns in alimestone massif seven miles north of Kuala Lumpur. All 39 specimens of B. m$er were collected in Cavern A (McClure, 1961), which is nearest the entrance of the cave system. These toads have fallen from above into the cave through small openings in the roof and are imprisoned within the cave. Examination and recording of stomach contents The toads were killed and preserved in 70% alcohol within one hour of capture, the abdominal walls being slit open to ensure rapid fixation of the viscera which were dissected later in the laboratory. Here, the snoutvent length of each specimen was recorded and the stomach removed and opened along its side of greater curvature. The stomach contents were removed and identified as far as possible under a low power binocular microscope, the food items being recorded in the following manner. For each stomach, the food organisms were counted individually and the volume of different food items determined according to the following procedure. All specimens of the same prey organism were placed in a 0.1 ml graduated cylinder after removing excess alcohol with filter paper. A known volume of 70% alcohol was then run in from a burette and the difference between the cylinder reading and the volume of added alcohol gave the Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

THE FOOD OF THE GIANT TOAD BUFO ASPER 63 volume of the food item being determined. In any stomach where only one or a few of the smaller items were found (e.g. acarines, small ants and Diptera), the volume of each item was calculated from a number of specimens of the same kind taken from several stomachs. The greatest linear dimension of almost all representative prey items were measured with a micrometer or, in the case of large organisms, with a centimetre rule. The number of empty stomachs and the number of stomachs containing any one organism were also recorded. The percentage representation of all the food items both by occurrence and volume were calculated. RESULTS Composition of the diet The number of empty stomachs and the details of occurrence, number and volumes of food items are shown for each locality in Table 2. Only a very small percentage of toads had empty stomachs ( and 5.1 7;). The most important dietary item of the toads from Templer Park was ants which were recovered from 100% of the stomachs and which made up the greater part by volume (44.9%) of the diet. Isoptera and Coleoptera were both common items of the diet at this locality, the former constituting the second most important food item in terms of bulk (22.8%). Blattaria, Dermaptera and Lepidoptera were not major food items. Table 2. Analysis of the food items of Bufo asper from Templer Park and Batu Caves Food items c Templer Park (54 toads) Empty stomach1 (%) P % of % of stomachs Total total containing no. of food item items volume Batu Caves (39 toads) Empty stomach2 (5.1%) c. % of % of stomachs Total total containing no. of food item items volume Orthoptera Blattaria Isoptera Hemiptera Dermaptera Lepidoptera (larvae) Lepidoptera (adults) Hymenoptera Formicidae (others) Coleoptera Diptera (larvae) Diptera (adults) Trichoptera (larvae) Acarina Araneae Phalangida Scorpionida Crustacea Diplopoda Chilopoda Gastropoda 11.3 3.8 37.7 18.9 3.8 5.7 5.7 100.0 37.7 9.4 3.8 5.7 6 1.5 2 2.5 4568 22.8 11 1.3 2 3 0.6 4 0.2 2277 44.9 1 35 8.6 1 1 2.9 1 0.1 1 0.3 6 0.5 1 4.2 2 3 9.5 1 0.1 10% 9 67.6 35.1 8.1 64.9 62.2 29.7 8.1 13.5 5.4 18.9 21.6 21.6 4 343 495 77 6 1207 67 35 4 28 2 11 19 14 1.71 55.95 25.65 0.99 0.30 3.61 3.93 2.50 0.31 0.51 0.21 1.46 1.86 1.oo Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

64 MRS P. Y. BERRY Unlike the Templer Park toads, those from Batu Caves consumed a great number of Blattaria (9 %of stomachs) and Dermaptera (67.6%). Together, these two items made up more than 80% of the total food volume (Table 2). Very small ants and Coleoptera occurred in over 60% of the stomachs but comprised only a small fraction of the total food volume. Similarly, Diptera larvae (mainly Stratiomyidae) (29.7%) and Lepidoptera larvae (mainly Tineidae) (35.1 %) occurred in a relatively high proportion of the stomachs. Isoptera which were eaten in large quantities by the Templer Park toads were completely lacking in the diet of the Batu Caves toads. Seasonal variation in food intake Figure 1 shows the total bimonthly rainfall together with the seasonal variation of the two major food items (ants and termites) consumed by the Templer Park toads. Both I962 1963 FIGURE 1. Bimonthly variation in rainfall, and two major food items of B. asper from Templer Park., Isoptera;, Hymenoptera (mostly ants). were found in the stomachs throughout the year. The number of termites ingested varied considerably in the bimonthly samples but could not be correlated with the total rainfall (Y = 0.063 ; P > 0.1). Comparisons of termite intake with rainy days and dry periods also fail to reveal any correlation. On the other hand, with the possible exception of the JuneJuly period, more ants were apparently eaten by the Templer Park toads during heavier rainfall periods than during the drier months (r = 0.746; 005 e P < 0.10) (Fig. 1). These included a high proportion of winged forms. Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

THE FOOD OF THE GIANT TOAD BUFO ASPER Food in relation to size There was a wide range in the size of food items ingested, from very small ants 2.0 mm in length to very large scolopendrid centipedes up to 50 mm long and polydesmid millipedes up to 60 mm long. More than SO% of the prey fell between the size range of 206.5 mm. This range includes most ants, termites, reduviid bugs, moth larvae and adults, many beetles, mites and Diptera. There appears to be a correlation between the size of the prey and the size of the predator (coefficient of concordance 0.507 ; P = 0.01). Relatively few prey greater than 95 mm length were eaten by toads of snoutvent length 80 mm or below. 65 Table 3. Numbers and percentages of prey of different sizes taken by toads of different snoutvent length Snoutvent No. of 2.03.5 4.06.5 7.09.5 10.012.5 13.015.5 16+ length toads No. % No. 'l/o No. % No. yo NO. % NO. % 40.160 60.180 80.1 1 00 100.1120 120.1140 140.1160 160+ Overall percentage 4 146 70.2 47 9 527 86.4 49 22 306 16.1 1338 35 165 6.5 1852 8 46 30.5 15 4 86 8 0 2 0 0 25 23.1 22.6 8.0 70.6 73.1 9.9 0 86.2 601 11 5.3 0 0 0 0 19 3.1 3 0.5 0 0 30 1.6 12 0.6 2 0.1 92 3.6 49 19 19 0.8 6 4.0 4 26 3 2.0 1 0.9 2 1.3 0 0 0 0 2 6.9 1 3.4 2.9 1.3 0.5 4 12 2.0 208 11.0 356 14.1 77 51.0 16 15.3 1 3.4 12.2 All measurements in millirnetres. DISCUSSION Many studies on the diet of amphibians have shown that selectivity, as well as availability, plays a role in predation. These include the works of Inger & Marx (1961) on Congo Anura, Berry (1965) on Singapore Anura, Berry (1966) on Amolops larutensis, Bragg (1967) on several Bufo species and Cott (1934) who pointed out that some amphibians refuse certain items of food though these may be made available. The only reference to the food of Bufo asper is by McClure (1965) and Bullock (1965). Their investigations were based on general observations and numerically small and unrepresentative samples of toads from Batu Caves. McClure reported that B. asper fed on Stratiomyidae, Blattidae and Tineidae while Bullock noted that the toads fed indiscriminately on the floor community. The result of this present survey shows that B. usper feeds exclusively on the ground and that its feeding, like that of many other amphibians, seems to depend on the abundance and availability of food. Differences have been noted in the diet of the toads from the two selected localities and these differences reflect the faunistic differences of the area. Although 144 species comprising four phyla and more than 25 orders of invertebrates were recorded from Batu Caves (McClure, 1965) and are potential sources of food for the toads, many of these were not included in the diet. Thus mites, which were found in masses on the bat guano of the cave floor, were eaten by relatively few toads whereas Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

66 MRS P. Y. BERRY spiders as well as Collembola, which occur freely on the guano in close company with ants, were completely lacking in the diet. The latter may have been excluded because of their very small size. The diet of the Templer Park toads included a wider variety of taxonomic groups than the Batu Caves toads (Table 2). Ants of all sizes from very small (2 mm) to very large (37 mm) proved to be by far the most important source of food quantitatively. Beside FIGURE 2. Per cent frequency of occurrence and % composition (by volume) of major food items found in the stomachs of B. asper and B. melanostictus. Solid black, B. asper from Batu Caves; open, B. asper from Templer Park; stipple, B. melanostictus from the Botanic Gardens. this, only termites contributed a significant volume. Coleoptera, although occurring in 37.7% of the stomachs, comprised only a small fraction of the total volume. Another important feature in the analysis of amphibian diet is to study the extent of interspecific variation in the diet. For each genus the questions to be raised are: Is the diet of all species within a genus made up of the same prey categories? Do the same prey groups make up the bulk of the food of each species in similar proportions? Figure 2 summarises the percentage frequency of occurrence and the percentage composition by volume of the diet of two Bufo species collected from three localities. The data for B. melanostictus were obtained from materials collected in 1962 from the Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

THE FOOD OF THE GIANT TOAD BUFO ASPER 67 Singapore Botanic Gardens. The Botanic Gardens included open grass, plant nurseries and patches of secondary forest. Despite the general dissimilarity of the terrain of the three areas, the kinds of food taken by the two species of Bufo showed several common features. Thus of the nine major taxonomic groups of food shown in Fig. 2, seven categories were ingested by both species from all three localities. However, Isoptera which occurred frequently in the stomachs of the Templer Park and Botanic Gardens toads were not ingested by the cave toads, whereas Gastropoda were not eaten by the Templer Park toads. In all three cases, ants, together with beetles were ingested by over 60% of the toads. Several workers have also shown that ants and Coleoptera constituted the major food item of other species of Bufo. Thus Weber, 1938 reported that 35 species of ants were eaten by B. marinus (L.) in Trinidad, and that ants constituted the bulk of all food in 76 % of the stomachs examined. Similarly Inger & Marx (1961) found that all four species of Bufo from the Congo fed heavily on ants and beetles. Studies on the diet of lower vertebrates have shown that in many cases, food intake and the composition of the diet change with the season. Recent examples of this kind include the works of Turner (1959) on Rana p. pretiosa Baird & Gir. in Wyoming, Inger & Marx (1961) on Anura, Avery (1966) on Lacerta vivipara Jacquin in England, and Sinha & Jones (1967) on freshwater eels in Wales. On the other hand, Berry (1966) showed that there was no seasonal variation in the diet of the torrent frog Amolops larutensis in Kuala Lumpur. Similarly, the results of this investigation indicate that food of most kinds was abundant and ingested by the toads throughout the year. The bimonthly fluctuations in the number of termites ingested varied considerably but attempts to correlate these fluctuations with rainfall fail to show any significant correlation (P > 0.1). It is suggested that these fluctuations depend on the chance encounter of termite nests by the toads. This is supported by the evidence that in almost all cases large quantities of earth and fragments of nest were ingested together with the termites. In the case of ants, there was an apparent increase in the number consumed in wetter than in drier months. This was probably due to the greater number of winged ants available to the toads after periods of heavier rainfall. The result of this survey shows that in B. usper there is a significant change in diet relative to size of the predator, and that there existed a clear lower limit to the size of food ingested; no food less than 2 mm in length was eaten. This was particularly noticeable in the case of acarines and collembolans. Only the larger mites were eaten whereas no collembolans were recovered from any of the stomachs examined. The upper size limit was probably represented by what could be swallowed by the toads and these included very large centipedes and millipedes. Selection of prey according to its size has been shown to occur in L. nigrops, K. pulchra, Microhyla heymonsii and M. butleri (Berry, 1965); in Amolops larutemis (Berry, 1966) and in Pelophryne signata (Boulenger) (Bullock, 1966). SUMMARY Examination of the stomach contents of 93 Bufo asper from two different localities shows that this species feeds on a wide range of invertebrates. In general, its diet depends on the availability and abundance of prey. Little or no marked seasonal variation in the diet was found. It is suggested that the bimonthly fluctuations in the number of Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206

68 MRS P. Y. BERRY termites ingested depend on the chance encounter of their nests and that more ants are eaten in wetter than in drier months. The relationship between predator and prey size and the interspecific variations in the diet of B. asper, B. melanostictus and other Bufo species are discussed. REFERENCES AVERY, R. A., 1966. Food and feeding habits of the Common lizard (Lacerta.i.ipara) in the west of Eng1and.J. Zool., Lond., 149: 115121. BERRY, P. Y., 1965. The diet of some Singapore Anura (Amphibia). Proc. 2001. Soc. Lond., 144: 163174. BERRY, P. Y., 1966. The food and feeding habits of the Torrent frog, Amolops 1arutensis.J. Zool., Lond., 149: 2W214. BERRY, P. Y. & BULLOCK, J. A., 1962. The food of the common Malayan toad, Bufo melanostictus Schneider. COP&, 1962: 736741. BRAGG, A. N., 1957. Some factors in the feeding of toads. Herpetologica, 13: 189191. BULLOCK, J. A., 1965. The ecology of Malaysian caves (and a note on the faunistic list from Batu Caves). Mulay. Nat.J., 19 (1): 5764. BULLOCK, J. A., 1966. Observations on the fauna of Pulau Tioman and Pulau Tulai. 7. The food of the amphibians and reptiles. Bull. natn. Mus. St. Singapore, 34: 8596. Con, H. B., 1934. Relative acceptability. Proc. ent. Sac. Land., 9: 3134. INGER, R. F. & MARX, H., 1961. The food of amphibians. Explor. Parc natn. Upemba Miss. G. F. de Witte, NO. 64: 186. MCCLURE, H. E., 1961. Batu Caves, Kuala Lumpur. Nature Conservation in Western M~l~ysia, 7378. Malayan Nature Society. MCCLURE, H. E., 1965. Microcosms of Batu Caves, and a List of Species collected at Batu Caves. Malay. Nat.J., 19 (1): 6574. SINHA, V. R. P. & JONES, J. W., 1967. On the food of the freshwater eels and their feeding relationship with the sa1rnonids.j. ZmZ., Lond., 153: 119137. TURN^, F. B., 1959. An analysis of the feeding habits of Ranap.pretiosa in Yellowstone Park, Wyoming. Am. Midl. Nat., 61: 403413. WEBER, N. A., 1938. The food of the Giant toad, Bufo marinus (L.), in Trinidad and British Guiana with special reference to the ants. Ann. ent. SOC. Am., 31 (4): 499503. Downloaded from https://academic.oup.com/zoolinnean/articleabstract/49/2/61/2664206