Abstract
Laboratory studies show that predatory cane toads (Bufo marinus) exhibit specialized toe-luring behavior that attracts smaller conspecifics, but field surveys of toad diet rarely record cannibalism. Our data resolve this paradox, showing that cannibalism is common under specific ecological conditions. In the wet–dry tropics of Australia, desiccation risk constrains recently metamorphosed toads to the edges of the natal pond. Juvenile toads large enough to consume their smaller conspecifics switch to a primarily cannibalistic diet (67% of prey biomass in stomachs of larger toads). Cannibalistic attack was triggered by prey movement, and (perhaps as an adaptive response to this threat) small (edible-sized) toads were virtually immobile at night (when cannibals were active). Smaller metamorphs were consumed more frequently than were larger conspecifics. The switch from insectivory to cannibalism reflects the high dry season densities of small conspecifics (in turn, due to desiccation-imposed constraints to dispersal) and the scarcity of alternative (insect) prey during dry weather. Our study pond (102 m in circumference) supported >400 juvenile toads, which consumed many metamorphs over the course of our study. Toads appear to be low-quality food items for other toads; in laboratory trials, juvenile toads that fed only on conspecifics grew less rapidly than those that ate an equivalent mass of insects. This effect was not due to parotoid gland toxins per se. Thus, cane toads switch to intensive cannibalism only when seasonal precipitation regimes increase encounter rates between large and small toads, while simultaneously reducing the availability of alternative prey.
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References
Alford RA (1999) Resource use, competition and predation. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, pp 240–278
Andrade MCB (1996) Sexual selection for male sacrifice in the Australian redback spider. Science 271:70–72
Andrade MCB (1998) Female hunger can explain variation in cannibalistic behavior despite male sacrifice in redback spiders. Behav Ecol 9:33–42
Anhold BR (1994) Cannibalism and early instar survival in a larval damselfly. Oecologia 99:60–65
Babbitt KJ, Meshaka WE Jr (2000) Benefits of eating conspecifics: effects of background diet on survival and metamorphosis in the Cuban Treefrog (Osteopilus septentrionalis). Copeia 2000:469–474
Bailey P (1976) Food of the marine toad, Bufo marinus, and six species of skink in cacao plantation in New Britain, Papua New Guinea. Aust Wildl Res 3:185–188
Baker MR (1979) The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidae) in amphibians. Can J Zool 57:161–178
Barton DP (1998) Dynamics of natural infections of Rhabdias cf. hylae (Nematoda) in Bufo marinus (Amphibia) in Australia. Parasitology 117:505–513
Bayliss P (1995) The ecology of post-metamorphic Bufo marinus in Central Amazonian Savanna, Brazil. PhD thesis. University of Queensland, Australia
Box HE (1925) Puerto Rican cane-grubs and their natural enemies. J Dept Agr Puerto Rico 9:291–356
Bragg AN (1940) Observations on the ecology and natural history of Anura. I. Habits, habitat and breeding of Bufo cognatus Say. Am Nat 74:322–349, 424–438
Bragg AN (1964) Further study on predation and cannibalism in spadefoot tadpoles. Herpetologica 20:17–24
Bragg AN, Weese AO (1950) Observations on the ecology and natural history of Anura. XIV. Growth rates and age at sexual maturity of Bufo cognatus under natural conditions in central Oklahoma. In: Bragg AN, Weese AO, Dundee HA, Fisher HT, Richards A, Clard CB (eds) Researches on the amphibians of Oklahoma. University of Oklahoma Press, Norman, pp 47–58
Brown HD (1972) The behaviour of newly hatched coccinellid larvae (Coleoptera: Coccinellidae). J Entomol Soc S Afr 35:149–157
Brown GP, Phillips BL, Webb JK, Shine R (2006) Toad on the road: use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biol Conserv 133:88–94
Bulkley RV (1970) Feeding interactions between adult bass and their offspring. Trans Am Fish Soc 99:732–738
Bury RB, Wheian AJ (1984) Ecology and management of the bullfrog. US Fish and Wildlife Service, Washington, DC US Fish Wildl Serv Res Publ 155
Buxbaum-Conradi H, Ewert JP (1999) Responses of single neurons in the toad’s caudal ventral striatum to moving visual stimuli and test of their efferent projection by extracellular antidromic stimulation/recording techniques. Brain Behav Evol 54:338–354
Caudell JN, James B, Lawie P (2000) Boiga irregularis (brown tree snake). Predation. Herpetol Rev 31:245
Chevalier JR (1973) Cannibalism as a factor in the first year survival of walleye in Oneida Lake. Trans Am Fish Soc 102:739–744
Child T (2007) The spatial and temporal ecology of metamorph cane toads (Chaunus marinus) in tropical Australia. BSc Honours thesis. University of Sydney, Australia
Child T, Phillips BL, Brown GP, Shine R (2008) The spatial ecology of cane toads (Chaunus marinus) in tropical Australia: why do metamorph toads stay near the water. Austral Ecol 33:630–640
Claverys JP, Havarstein LS (2007) Cannibalism and fratricide: mechanisms and raisons d’etre. Nature Rev Microbiol 5:219–229
Cohen MP, Alford RA (1993) Growth, activity and patterns of recently metamorphosed Bufo marinus. Wildl Res 20:1–13
Collins JP, Cheek JE (1983) Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum. Am Zool 23:77–84
Collins JP, Holomuzki JR (1984) Intraspecific variation in diet within and between trophic morphs in larval tiger salamanders (Ambystoma tigrinum nebulosum). Can J Zool 62:168–174
Covacevich J, Archer M (1975) The distribution of the cane toad, Bufo marinus, in Australia and its effects on indigenous vertebrates. Mem Qld Mus 17:305–310
Crump ML (1986) Cannibalism by younger tadpoles: another hazard of metamorphosis. Copeia 1986:1007–1009
Crump ML (1992) Cannibalism in amphibians. In: Elgar MA, Crespi BJ (eds) Cannibalism: ecology and evolution in diverse taxa. Oxford University Press, Oxford, pp 256–276
Cunningham JD (1962) Observations on the natural history of the California toad, Bufo californicus Camp. Herpetologica 17:255–260
Dexter RR (1932) The food habits of the imported cane toad, Bufo marinus, in the sugar cane sections of Puerto Rico. Int Soc Sugar Cane Tech Bull 74:2–6
Dole JW, Rose BB, Tachiki KH (1981) Western toads (Bufo boreas) learn odor of prey insects. Herpetologica 37:63–68
Duellman WE, Trueb L (1994) Biology of amphibians. McGraw-Hill, New York
Dushin AI (1975) Diet of two frog species in fishery ponds of the Mordovian (ASSR). Soviet J Ecol 5:87–90
Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73:321–346
Forney JL (1974) Interactions between yellow perch abundance, walleye predation, and survival of alternate prey in Oneida Lake, New York. Trans Am Fish Soc 103:15–24
Forster LM (1992) The stereotyped behaviour of sexual cannibalism in Latrodectus hasselti Thorell (Araneae: Theridiidae), the Australian redback spider. Aust J Zool 40:1–11
Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106
Freeland WJ, Kerin SH (1991) Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl Res 18:431–443
Freeland WJ, Delvinquier BLJ, Bonnin B (1986) Food and parasitism of the cane toad, Bufo marinus, in relation to time since colonization. Aust Wildl Res 13:489–499
Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:1–370
Gajdusek DC, Alpers M (1972) Genetic studies in relation to Kuru. I. Cultural, historical and demographic background. Am J Hum Genet (Suppl) 24:1–38
Greenlees MJ, Brown GP, Webb JK, Phillips BL, Shine R (2006) Effects of an invasive anuran (the cane toad, Bufo marinus) on the invertebrate fauna of a tropical Australian floodplain. Anim Conserv 9:431–438
Hagman M, Shine R (2008) Deceptive digits: the functional significance of toe-waving by cannibalistic cane toads (Chaunus marinus). Anim Behav 75:123–131
Hinckley AD (1963) Diet of the giant toad, Bufo marinus (L), in Fiji. Herpetologica 18:253–259
Holomuzki JR (1986) Intraspecific predation and habitat use by tiger salamanders (Ambystoma tigrinum nebulosum). J Herpetol 20:439–441
Huey RB (1980) Sprint velocity of tadpoles (Bufo boreas) through metamorphosis. Copeia 1980:537–540
Illingworth JF (1941) Feeding habits of Bufo marinus. Proc Haw Ent Soc 11:51
Kaddou IK (1960) The feeding behaviour of Hippodamia quinquesignata (Kirby) larvae. Univ Calif Pub Entomol 16:181–230
Kelehear C (2007) The effects of lung nematodes (Rhabdias cf. hylae) on metamorph cane toads (Chaunus marinus), and implications for biological control. BSc Honours thesis. University of Sydney, Australia
Kinoshita M (1998) Effects of time-dependent intraspecific competition on offspring survival in the butterfly, Anthocharis scolymus (L.) (Lepidoptera: Pieridae). Oecologia 114:31–33
Kirn AJ (1949) Cannibalism among Rana pipiens berlandieri, and possibly by Rana catesbiana, near Somerset, Texas. Herpetologica 5:84
Korschgen LJ, Moyle DL (1955) Food habits of the bullfrog in central Missouri farm ponds. Am Midl Nat 54:332–341
Lannoo MJ, Bachmann MD (1984) Aspects of cannibalistic morphs in a population of Ambystoma t. tigrinum larvae. Am Midl Nat 112:103–109
Lannoo MJ, Lowcock L, Bogart JP (1989) Sibling cannibalism in non-cannibal morph Ambystoma tigrinum larvae and its correlation with high growth rates and early metamorphosis. Can J Zool 67:1911–1914
Larson KL, Duffy W, Johnson E, Donovan MF, Lannoo MJ (1999) “Paedocannibal” morph barred tiger salamanders (Ambystoma tigrinum mavortium) from east central South Dakota with comments on the origin of cannibal morph eastern tiger salamanders (A. t. tigrinum) from northwest Iowa. Am Midl Nat 141:124–139
Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic and Scientific Publishing, Otley, West Yorkshire
Llewelyn J, Phillips BL, Shine R. (2008) Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecol: in press
Lourdais O, Brischoux F, Shine R, Bonnet X (2005) Adaptive maternal cannibalism in snakes (Epicrates cenchria maurus, Boidae). Biol J Linn Soc 84:767–774
Macneil C, Dick JTA, Hatcher MJ, Fielding NJ, Hume KD, Dunn AM (2003) Parasite transmission and cannibalism in an amphipod (Crustacea). Int J Parasitol 33:795–798
Manica A (2002) Filial cannibalism in teleost fish. Biol Rev 77:261–277
Matsushima N, Kawata M (2005) The choice of oviposition site and the effects of density and oviposition timing on survivorship in Rana japonica. Ecol Res 20:81–86
Matuschka FR, Bannert B (1989) Recognition of cyclic transmission of Sarcocystis stehlinii n. sp. in the Gran Canarian giant lizard. J Parasitol 75:383–387
Niven BS, Stewart MG (1982) The precise environment of some well known animals. VII. The cane toad (Bufo marinus), vol. 3. School of Australian Environmental Studies, Griffith University, Brisbane AES Working Paper
Oliver JA, Shaw CE (1953) The amphibians and reptiles of the Hawaiian Islands. Zoologica 38:65–95
Pack HJ (1922) Toads in regulating insect outbreaks. Copeia 1922:46–47
Petranka JW, Thomas DAG (1995) Explosive breeding reduces egg and tadpole cannibalism in the wood frog, Rana sylvatica. Anim Behav 50:731–739
Pfennig DW (1997) Kinship and cannibalism. BioScience 47:667–675
Pfennig DW (1999) Cannibalistic tadpoles that pose the greatest threat to kin are most likely to discriminate kin. Proc R Soc Lond B 266:57–61
Pfennig DW, Collins JP (1993) Kinship affects morphogenesis in cannibalistic salamanders. Nature 362:836–838
Pfennig DW, Frankino WA (1997) Kin mediated morphogenesis in facultatively cannibalistic tadpoles. Evolution 51:1993–1999
Pfennig DW, Ho SG, Hoffman EA (1998) Pathogen transmission as a selective force against cannibalism. Anim Behav 55:1255–1261
Pfennig DW, Sherman PW, Collins JP (1994) Kin recognition and cannibalism in polyphenic salamanders. Behav Ecol 5:225–232
Phillips BL, Shine R (2005) The morphology, and hence impact, of an invasive species (the cane toad, Bufo marinus): changes with time since colonization. Anim Conserv 8:407–413
Phillips BL, Brown GP, Greenlees M, Webb JK, Shine R (2007) Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecol 32:169–176
Pippet JR (1975) The marine toad, Bufo marinus, in Papua New Guinea. PNG Agr J 26:23–30
Pizzatto L, Child T, Shine R (2008) Why be diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics. Behav Ecol: in press. doi:10.1093/beheco/arn060
Poelman EH, Dicke M (2006) Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evol Ecol 21:215–227
Polis GA (1980) The effect of cannibalism on the demography and activity of a natural population of desert scorpions. Behav Ecol Sociobiol 7:25–35
Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251
Polis GA, Myers CA (1985) A survey of intraspecific predation among reptiles and amphibians. J Herpetol 19:99–107
Quesnel VC (1986) An unusual prey for the marine toad, Bufo marinus 1985–1986. Living World 1986:25
Rogers PC (1996) Rana catesbeiana (bullfrog) predation. Herp Rev 27:75
Rose FL, Armentrout D (1976) Adaptive strategies of Ambystoma tigrinum inhabiting the Llano Estacado of West Texas. J Anim Ecol 45:713–729
Rosen P (2007) Rana yavapaiensis (Lowland Leopard Frog). Larval cannibalism. Herpetol Rev 38:195–196
Roth G, Wiggers W (1983) Responses of the toad Bufo bufo (L.) to stationary prey stimuli. Zeitschrift fur Tierpsychol 61:225–234
Sasaki T, Iwahashi O (1995) Sexual cannibalism in an orb-weaving spider Argiope aemula. Anim Behav 49:1119–1121
Schwalbe R, Rosen PC (1988) Preliminary report on effects of bullfrogs on wetland herpetofauna in southeastern Arizona. In: Szaro R, Severson K, Patton D (eds) Management of amphibians, reptiles and small mammals in North America. US Forest Service, Washington, DC, pp 166–173 General Technical Report RM-166
Scott NJ Jr, Aquino AL (2005) It’s a frog-eat-frog world in the Paraguayan Chaco: food habits, anatomy, and behavior of the frog-eating anurans. In: Donnelly MA, Crother BI, Guyer C, Wake MH, White ME (eds) Ecology and evolution in the tropics: a herpetological perspective. University of Chicago Press, Chicago, pp 243–259
Shankman P (1969) Le Rôti et le Bouilli: Lévi-Strauss’ theory of cannibalism. Am Anthropol 71:54–69
Sievert G, Sievert L (2005) A field guide to Oklahoma’s amphibians and reptiles. Oklahoma Department of Wildlife Conservation, Oklahoma
Smyth JD, Smyth MM (1980) Frogs as host-parasite systems I. An introduction to parasitology through the parasites of Rana temporaria, R. esculenta and R. pipiens. Macmillan Press, London
Stuart NJ (1993) Rana catesbeiana cannibalism. Herp Rev 24:103
Summers K (1989) Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus. Anim Behav 37:797–805
Thibault RE (1974) Genetics of cannibalism in a viviparous fish and its relationship to population density. Nature 251:138–140
Toft CA (1985) Resource partitioning in amphibians and reptiles. Copeia 1985:1–21
Urban MC, Phillips BL, Skelly DK, Shine R (2007) The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc R Soc Lond Ser B 274:1413–1419
Wassersug RJ, Sperry DG (1977) The relationships of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58:830–839
Wildy EL, Chivers DP, Kiesecker JM, Blaustein AR (1998) Cannibalism enhances growth in larval long-toed salamanders (Ambystoma macrodactylum). J Herpetol 32:286–289
Wiseman KD, Bettaso J (2007) Rana boylii (Foothill Yellow-Legged Frog). Cannibalism and predation. Herpetol Rev 38:193
Yom-Tov Y (1974) The effect of food and predation on breeding density and success, clutch size and laying date of the crow Corvus corone L.: an experimental approach. J Anim Ecol 43:479–498
Zug GR, Zug PB (1979) The marine toad Bufo marinus: a natural history resumé of native populations. Smithsonian Contrib Zool 284:1–52
Zug GR, Lindgren E, Pippet JR (1975) Distribution and ecology of the marine toad, Bufo marinus, in Papua New Guinea. Pac Sci 29:31–50
Acknowledgements
We thank Team Bufo and the staff of Beatrice Hill Farm for support and encouragement, Barry Scott (Parks and Wildlife Commission of the Northern Territory) and the Northern Territory Lands Corporation for access to laboratory facilities, Greg Brown for unpublished data, and Mattias Hagman and especially Travis Child for stimulating our interest in cannibalism in toads and for many discussions. Christa Beckmann, Michael Crossland, and Matt Greenlees helped with fieldwork, Christa Beckmann took some of the photographs, and the Australian Research Council (RS) and CAPES (LP) provided financial support. All procedures were approved by the University of Sydney Animal Ethics Committee (approval L04/5-2007/3/4515).
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Pizzatto, L., Shine, R. The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behav Ecol Sociobiol 63, 123–133 (2008). https://doi.org/10.1007/s00265-008-0642-0
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DOI: https://doi.org/10.1007/s00265-008-0642-0