Abstract
Exploratory behavior can be a key component of survival in novel or changing environments, ultimately determining population establishment. While many studies have investigated the behavior of wild animals in response to novel food items or objects, our understanding of how they explore novel environments is limited. Here, we examine how experience affects the foraging behavior of a species with high invasive potential. In particular, we investigate the movement and behavior of cane toads as a function of experience in a novel environment, and how the presence of food modulates exploration. Cane toads, from a population in their native range, were repeatedly tested in a large, naturalistic arena with or without food present. Both groups exhibited significant but different changes in exploratory behavior. While toads in an environment without food reduced exploratory behavior over trials, those with food present increased both food intake per trial and the directness of their paths to food, resulting in fewer approaches to food patches over time. Our results suggest that cane toads learn patch location and provide preliminary evidence suggesting toads use spatial memory, not associative learning, to locate food. In sum, we show that with experience, cane toads alter their behavior to increase foraging efficiency. This study emphasizes the role of learning in foraging in cane toads, a characteristic that may have facilitated their success as invaders.
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References
Alexander TR (1965) Observations on the feeding behavior of Bufo marinus (Linne). Herpetologica 20:255–259
Ayers CA, Armsworth PR, Brosi BJ (2015) Determinism as a statistical metric for ecologically important recurrent behaviors with trapline foraging as a case study. Behav Ecol Sociobiol 69:1395–1404
Benhamou S (2004) How to reliably estimate the tortuosity of an animal’s path: straightness, sinuosity, or fractal dimension? J Theor Biol 229:209–220
Bilbo SD, Day LB, Wilczynski W (2000) Anticholinergic effects in frogs in a Morris water maze analog. Physiol Behav 69:351–357
Brattstrom BH (1990) Maze learning in the fire-bellied toad, Bombina orientalis. J Herpetol 24:44–47
Candler SA, Bernal XE (2015) Differences in neophobia between cane toads from introduced and native populations. Behav Ecol 26:97–104
Cheng K, Jeffery KJ (2017) Spatial cognition. In: Call J (ed) APA handbook of comparative psychology. American Psychological Association, Washington, DC, pp 463–483
Crane AL, Mathis A (2011) Landmark learning by the Ozark zigzag salamander, Plethodon angusticlavius. Curr Zool 57:485–490
Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. TREE 20:187–193
Dall’Antonia L, Sinsch U (2001) In search of water: orientation behaviour of dehydrated natterjack toads, Bufo calamita. Anim Behav 61:617–629
Daneri MF, Casanave E, Muzio RN (2011) Control of spatial orientation in terrestrial toads (Rhinella arenarum). J Comp Psychol 125:296–307
Davis MA (2009) Invasion biology. Oxford University Press, Oxford
Deecke VB (2006) Studying marine mammal cognition in the wild: a review of four decades of playback experiments. Aquat Mamm 32:461–482
Devenport L, Humphries T, Devenport J (1994) Spatial navigation in natural habitats by ground-dwelling sciurids. Anim Behav 47:727–729
Devenport L, Humphries T, Devenport J (1998) Future value and patch choice in least chipmunks. Anim Behav 55:1571–1581
Drea CM (2006) Studying primate learning in group contexts: tests of social foraging, response to novelty, and cooperative problem solving. Methods 38:162–177
Durier V, Rivault C (2001) Effects of spatial knowledge and feeding experience on foraging choices in German cockroaches. Anim Behav 62:681–688
Ewert JP (1980) Neuroethology: an introduction to the neurophysiological fundamentals of behavior. Springer, Berlin
Ewert JP (2004) Motion perception shapes the visual world of amphibians. In: Prete FR (ed) Complex worlds from simpler nervous systems. MIT Press, Cambridge, pp 117–160
Fontanet X, Horta N (1989) Capacidad de aprendizaje en Euproctus asper (Duges 1852) (Amphibia: Caudata). Treballs d’ictiologia i herpetologia. X. Fontanet and N. Horta, Soc. Cat. Ictio. Herpetology 2:134–146
Gibson KW, Hall CL, Kramer DL (2006) Time-concentrated sampling: a simple strategy for information gain at a novel, depleted patch. Can J Zool 84:1513–1521
Grubb JC (1976) Maze orientation by Mexican toads, Bufo valliceps (Amphibia, Anura, Bufonidae), using olfactory and configurational cues. J Herpetol 10:97–104
Hall CS (1934) Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol 18:385–403
Hayes KJ, Thompson R, Hayes C (1953) Discrimination learning set in chimpanzees. J Comp Physiol Psychol 46:99–104
Hoffmann G (1983) The random elements in the systematic search behaviour of the desert isopod Hemilepistus reaumuri. Behav Ecol Sociobiol 31:81–92
Klein S, Pasquaretta C, Barron AB, Devaud J-M, Lihoreau M (2017) Inter-individual variability in the foraging behaviour of traplining bumblebees. Sci Rep 7:4561
Krakauer T (1968) The ecology of the neotropical toad, Bufo marinus, in South Florida. Herpetologica 24:214–221
Lever C (2001) The cane toad: the history and ecology of a successful colonist. Westbury Academic & Scientific Publishing, Otley
Lindstrom T, Brown GP, Sisson SA, Phillips BL, Shine R (2013) Rapid shifts in dispersal behavior on an expanding range edge. Proc Nat Acad Sci 110:13452–13456
Lüddecke H (2003) Space use, cave choice, and spatial learning in the dendrobatid frog Colostethus palmatus. Amphib-Reptil 24:37–46
Martof B (1962) Some observations on the feeding of Fowler’s toad. Copeia 1962(2):439
McCann S, Greenlees MJ, Newell D, Shine R (2014) Rapid acclimation to cold allows the cane toad (Rhinella marina) to invade montane areas within its Australian range. Func Ecol 28:1166–1174
McDonald JH (2009) Handbook of biological statistics, 2nd edn. Sparky House Publishing, Baltimore
McGill TE (1960) Response of the Leopard Frog to electric shock in an escape-learning situation. J Comp Physiol Psychol 53:443–445
Mead AP (1957) A quantitative method for the analysis of exploratory behavior in the rat. Anim Behav 8:19–31
Mettke-Hofmann C, Winklerà H, Leisler B (2002) The significance of ecological factors for exploration and neophobia in parrots. Ethology 108:249–272
Olton DS, Collison C, Werz MANN (1977) Spatial memory and radial arm maze performance of rats. Learn Motiv 8:289–314
Pašunokis A, Trenkwalder K, Ringler M, Ringler E, Mangione R, Steininger J, Warrington I, Hödl W (2016) The significance of spatial memory for water finding in a tadpole-transporting frog. Anim Behav 116:89–98
Paulissen MA (2008) Spatial learning in the little brown skink, Scincella lateralis: the importance of experience. Anim Behav 76:135–141
Pettit LJ, Greenlees MJ, Shine R (2017) The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments? Behav Ecol Sociobiol 71:1–15
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
Poirier FE, Hussey LK (1982) Nonhuman primate learning: the importance of learning from an evolutionary perspective. Anthropol Educ Q 13:133–148
Poucet B, Chapuis N, Durup M, Thinus-Blanc C, Neurophysiologie ID (1986) A study of exploratory behavior as an index of spatial knowledge in hamsters. Control 14:93–100
Pritchard DJ, Healy SD (2017) Homing and navigation. In: Call J (ed) APA handbook of comparative psychology. American Psychological Association, Washington, DC, pp 485–508
Punzo F, Bottrell J (2001) Spatial learning in the lynx spider, Oxyopes salticus Hentz (Araneae: Oxyopidae). Bull Br Arachnol Soc 12:105–109
Reynolds AM, Smith AD, Menzel R, Greggers U, Reynolds DR, Riley JR (2007a) Displaced honey bees perform optimal scale-free search flights. Ecology 88:1955–1961
Reynolds AM, Smith AD, Reynolds DR, Carreck NL, Osborne JL (2007b) Honeybees perform optimal scale-free searching flights when attempting to locate a food source. J Exp Biol 210:3763–3770
Russell JC, McMorland AJC, MacKay JWB (2010) Exploratory behaviour of colonizing rats in novel environments. Anim Behav 79:159–164
Schultheiss P, Cheng K, Reynolds AM (2015) Searching behavior in social Hymenoptera. Learn Motiv 50:59–67
Simon P, Dupuis R, Costentin J (1993) Thigmotaxis as an index of anxiety in mice: influence of dopaminergic transmissions. Behav Brain Res 61:59–64
Sinsch U (2006) Orientation and navigation in Amphibia. Mar Freshw Behav Physiol 39:65–71
Sol D (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci USA 102:5460–5465
Stynoski JL (2009) Discrimination of offspring by indirect recognition in an egg-feeding dendrobatid frog, Oophaga pumilio. Anim Behav 78:1351–1356
Suboski MD (1992) Releaser-induced recognition learning by amphibians and reptiles. Anim Learn Behav 20:63–82
Van Bocxlaer I, Loader SP, Roelants K, Biju SD, Menegon M, Bossuyt F (2010) Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327:679–682
Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504
Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40:500–505
Zamora AJ, Lopez ME, Vila J, Cabrera R (2012) Cantidad, lugar y tiempo determinan estrategias de búsqueda de alimento de paloma. Acta Investig Psicol 2:858–867
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River
Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. In Smithsonian contributions to zoology. Smithsonian Institution Press, Washington, DC
Acknowledgements
Funding was provided by the Association of Biologists at Texas Tech University, and the HHMI Center for the Integration of Science Education and Research to AJM. We are grateful to the Smithsonian Tropical Research Institute for use of lab facilities and equipment, to Rich Strauss for his advice concerning statistical methods, and to Damond Kyllo for his cane toad drawing. H. Miller, N. Lewis, M. Hein, M. Harris, E. Braverman, and H. Russon provided invaluable help scoring toad behavior on videos. Two anonymous reviewers and K. Cheng provided constructive criticisms and suggestions that greatly improved the quality of this study.
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Illustration of escape attempts. Three different instances of a toad trying to escape the arena are shown (MP4 852 kb)
Video recorded during preliminary trials illustrating the behavior of toads when eating. In contrast to the design in the experiment of the study, the toad is here shown eating from a bowl in which multiple mealworms were presented. This set-up was not selected given that when mealworms crawl on each other, they produce acoustic cues that could be perceived by the toad (MP4 336 kb)
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Miller, A.J., Page, R.A. & Bernal, X.E. Exploratory behavior of a native anuran species with high invasive potential. Anim Cogn 21, 55–65 (2018). https://doi.org/10.1007/s10071-017-1138-y
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DOI: https://doi.org/10.1007/s10071-017-1138-y