Evolutionary shifts in anti-predator responses of invasive cane toads (Rhinella marina)

  • Cameron M. Hudson
  • Gregory P. Brown
  • Richard Shine
Original Article


A potential prey item’s response to encountering a predator depends on aspects of the predator (e.g., its locomotor capacity), the local environment (e.g., proximity to shelter) and the physiological state of the prey item, but in addition, anti-predator tactics also vary geographically among different populations within wide-ranging species. Using standardised trials, we tested responses of cane toads (Rhinella marina) to being placed on a laboratory runway and encouraged to flee. Overall, the toads least capable of rapid locomotion were the ones most likely to respond to simulated predator attack by exuding toxins rather than attempting to escape. A toad’s willingness to move down the runway and its propensity to exude toxin from the parotoid glands rather than fleeing were repeatable in successive trials and influenced by the animal’s location of origin, morphology, previous experience, and parentage. We found that specimens from Australia were more willing to flee than were those from the native range (French Guiana) or Hawai’i; larger toads, and those with relatively longer legs, were more willing to flee; captive-raised toads were less willing to flee and more willing to exude toxin. Captive-raised offspring resembled their wild-caught parents both in propensity to run and in propensity to exude toxin. Thus, geographic divergence among cane toad populations in anti-predator responses reflects a complex combination of processes, including both developmental plasticity and heritability.

Significance statement

The process of colonising novel environments exposes an organism to a host of different predators that exert selection on morphology, behaviour and physiology. Over time, this can lead to the evolution of novel phenotypes that are adapted to local conditions. Anthropogenically facilitated biological invasions provide a unique opportunity to study how species respond to colonisation of new environments. Here, we studied geographic variation in cane toad (Rhinella marina) anti-predator behaviours from a range of locations (including invasive and native populations) using standardised trials. Our results suggest that invasive Australian cane toads have undergone a shift in their anti-predator response, becoming more willing to flee than are conspecifics from other areas. Location of origin, morphology, prior experience and parentage all played a role in shaping a toad’s anti-predator response, suggesting that the behaviour represents a combination of plastic and heritable variation.


Anti-predator response Bufo marinus Invasive species Locomotion Morphology Rhinella marina 


  1. Alford RA, Cohen MP, Crossland MR, Hearnden MN, James D, Schwarzkopf L (1995) Population biology of Bufo marinus in northern Australia. In: Finlayson M (ed) Wetland research in the wet-dry tropics of Australia. Supervising Scientist Report No. 101, Office of the Supervising Scientist, Canberra, ACT, pp 173–181Google Scholar
  2. Almeida PG, Felsemburgh FA, Azevedo RA, Brito-Gitirana L (2007) Morphological re-evaluation of the parotoid glands of Bufo ictericus (Amphibia, Anura, Bufonidae). Contrib Zool 76:145–152Google Scholar
  3. Amiel JJ, Lindström T, Shine R (2014) Egg incubation effects generate positive correlations between size: speed and learning ability in young lizards. Anim Cogn 17:337–347CrossRefPubMedGoogle Scholar
  4. Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374CrossRefPubMedPubMedCentralGoogle Scholar
  5. Amo L, Lopez P, Martın J (2007) Refuge use: a conflict between avoiding predation and losing mass in lizards. Physiol Behav 90:334–343CrossRefPubMedGoogle Scholar
  6. Arduino PJ, Gould JL (1984) Is tonic immobility adaptive? Anim Behav 32:921–923CrossRefGoogle Scholar
  7. Atkins R, Blumstein DT, Moseby KE, West R, Hyatt M, Letnic M (2016) Deep evolutionary experience explains mammalian responses to predators. Behav Ecol Sociobiol 70:1755–1763CrossRefGoogle Scholar
  8. Barbosa A, Allen JJ, Mäthger LM, Hanlon RT (2012) Cuttlefish use visual cues to determine arm posture for camouflage. Proc R Soc Lond B 279:84–90CrossRefGoogle Scholar
  9. Bestion E, Teyssier A, Aubret F, Clobert J, Cote J (2014) Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal. Proc R Soc B 281:20140701CrossRefPubMedPubMedCentralGoogle Scholar
  10. Broom M, Ruxton GD (2005) You can run—or you can hide: optimal strategies for cryptic prey against pursuit predators. Behav Ecol 16:534–540CrossRefGoogle Scholar
  11. Brodie ED Jr, Gibson LS (1969) Defensive behavior and skin glands of the Northwestern Salamander, Amybstoma gracile. Herpetologica 25:187–194Google Scholar
  12. Brodie ED III (1989) Genetic covariances between morphology and anti-predator behavior in natural populations of the garter snake Thamnophis ordinoides. Nature 342:542–543CrossRefPubMedGoogle Scholar
  13. Brodie ED III (1993) Homogeneity of the genetic variance-covariance matrix for anti-predator traits in two natural populations of the garter snake Thamnophis ordinoides. Evolution 47:844–854CrossRefPubMedGoogle Scholar
  14. Brodie ED III, Russell NH (1999) The consistency of individual differences in behaviour: temperature effects on antipredator behaviour in garter snakes. Anim Behav 57:445–451CrossRefPubMedGoogle Scholar
  15. Brown GP, Kelehear C, Shilton CM, Phillips BL, Shine R (2015) Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations. Biol J Linn Soc 116:748–760CrossRefGoogle Scholar
  16. Brown GP, Shine R (2004) Effects of reproduction on the anti-predator tactics of snakes (Tropidonophis mairii, Colubridae). Behav Ecol Sociobiol 56:257–262Google Scholar
  17. Burger J, Gochfield M, Saliva JE, Gochfield D, Gochfield D, Morlaes H (1989) Antipredator behavior in nesting zenaida doves (Zenaida aurita): parental investment or offspring vulnerability. Behaviour 111:129–143CrossRefGoogle Scholar
  18. Cannon WB (1929) Bodily changes in pain, hunger, fear, and rage. Appleton-Century-Crofts, New York, USAGoogle Scholar
  19. Caro T (2005) Anti-predator defenses in birds and mammals. University of Chicago Press, Chicago, IL, USAGoogle Scholar
  20. Chivers DP, Mitchell MD, Lucon-Xiccato T, Brown GE, Ferrari MCO (2016) Background risk influences learning but not generalization of predators. Anim Behav 121:185–189CrossRefGoogle Scholar
  21. Choi I, Shim JH, Ricklefs RE (2003) Morphometric relationships of take-off speed in anuran amphibians. J Exp Zool 299:99–102CrossRefGoogle Scholar
  22. Cooper W (2015) Age affects escape behavior by the zebra-tailed lizard (Callisaurus draconoides) more strongly than in other lizards. Amphibia-Reptilia 36:37–44CrossRefGoogle Scholar
  23. Cooper WE Jr (2000) Effect of temperature on escape behaviour by an ectothermic vertebrate, the keeled earless lizard (Holbrookia propinqua). Behaviour 137:1299–1315CrossRefGoogle Scholar
  24. Cooper WE Jr, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67CrossRefPubMedGoogle Scholar
  25. Cox JG, Lima SL (2006) Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680CrossRefPubMedGoogle Scholar
  26. Cushing BS (1985) Estrous mice and vulnerability to weasel predation. Ecology 66:1976–1978CrossRefGoogle Scholar
  27. de Barros FC, de Carvalho JE, Abe AS, Kohlsdorf T (2009) Fight versus flight: the interaction of temperature and body size determines antipredator behaviour in tegu lizards. Anim Behav 79:83–88CrossRefGoogle Scholar
  28. Donnelly WA, Dill LM (1984) Evidence for crypsis in coho salmon, Oncorhynchus kisutch (Walbaum), parr: substrate colour preference and achromatic reflectance. J Fish Biol 25:183–195CrossRefGoogle Scholar
  29. Durso AM, Mullin SJ (2013) Intrinsic and extrinsic factors influence expression of defensive behaviour in plains hog-nosed snakes (Heterodon nasicus). Ethology 120:140–148CrossRefGoogle Scholar
  30. Dutour M, Lena JP, Lengagne T (2016) Mobbing behaviour varies according to predator dangerousness and occurrence. Anim Behav 119:119–124CrossRefGoogle Scholar
  31. Edelaar P, Serrano D, Carrete M, Blas J, Potti J, Tella JL (2012) Tonic immobility is a measure of boldness toward predators: an application of Bayesian structural equation modeling. Behav Ecol 23:619–626CrossRefGoogle Scholar
  32. Eklöv P, Werner EE (2000) Multiple predator effects on size-dependent behaviour and mortality of two species of anuran larvae. Oikos 88:250–258CrossRefGoogle Scholar
  33. Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol S 39:387–413CrossRefGoogle Scholar
  34. Easteal S (1981) The history of introductions of Bufo marinus (Amphibia: Anura); a natural experiment in evolution. Biol J Linn Soc 16:93–113CrossRefGoogle Scholar
  35. Ewell AH, Cullen JM, Woodruff ML (1981) Tonic immobility as a predator-defense in the rabbit (Oryctolagus cuniculus). Behav Neural Biol 31:483–489CrossRefGoogle Scholar
  36. Ferrari MCO, Messier F, Chivers DP (2008) Larval amphibians learn to match antipredator response to temporal patterns of risk. Behav Ecol 19:980–983CrossRefGoogle Scholar
  37. Gifford ME, Mahler DL, Herrel A (2008) The evolution of locomotor morphology, performance, and anti-predator behavior among populations of Leiocephalus lizards from the Dominican Republic. Biol J Linn Soc 93:445–456CrossRefGoogle Scholar
  38. Gomes FR, Rezende EL, Grizante MB, Navas CA (2009) The evolution of jumping performance in anurans: morphological correlates and ecological implications. J Evol Biol 22:1088–1097CrossRefPubMedGoogle Scholar
  39. Greene HW (1988) Anti-predator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, ecology B. Defense and life history, volume 16. Alan R. Liss Inc., New York, USA, pp 1–152Google Scholar
  40. Gregory PT, Isaac LA, Griffiths RA (2007) Death feigning by grass snakes (Natrix natrix) in response to handling by human predators. J Comp Psychol 121:123–129CrossRefPubMedGoogle Scholar
  41. Gruber J, Brown G, Whiting MJ, Shine R (2017) Geographic divergence in dispersal-related behaviour in cane toads from range-front versus range-core populations in Australia. Behav Ecol Sociobiol 71:38CrossRefGoogle Scholar
  42. Hagman M, Hayes R, Capon R, Shine R (2009) Alarm cues experienced by cane toad tadpoles affect post metamorphic morphology and chemical defences. Funct Ecol 23:126–132CrossRefGoogle Scholar
  43. Hagman M, Löwenborg K, Shine R (2015) Determinants of anti-predator tactics in hatchling grass snakes (Natrix natrix). Behav Process 113:60–65CrossRefGoogle Scholar
  44. Hawlena D, Boochnik R, Abramsky Z, Bouskila A (2006) Blue tail and striped body: why do lizards change their infant costume when growing up? Behav Ecol 17:889–896CrossRefGoogle Scholar
  45. Hernández SE, Sernia C, Bradley AJ (2016) Adrenocortical function in cane toads from different environments. Comp Biochem Physiol A 195:65–72CrossRefGoogle Scholar
  46. Hertz PE, Huey RB, Nevo E (1982) Fight versus flight: body temperature influences defensive responses of lizards. Anim Behav 30:676–679CrossRefGoogle Scholar
  47. Hettyey A, Tóth Z, Van Buskirk J (2014) Inducible chemical defences in animals. Oikos 123:1025–1028CrossRefGoogle Scholar
  48. Hoagland H (1928) On the mechanism of tonic immobility in vertebrates. J Gen Physiol 11:715–741CrossRefPubMedPubMedCentralGoogle Scholar
  49. Hopkins GR, Migabo SW (2010) Antipredator skin secretions of the long-toed salamander (Ambystoma macrodactylum) in its northern range. J Herpetol 44:627–633CrossRefGoogle Scholar
  50. Hossie TJ, Sherratt TN (2013) Defensive posture and eyespots deter avian predators from attacking caterpillar models. Anim Behav 86:383–389CrossRefGoogle Scholar
  51. Hostetler JR, Cannon MS (1974) The anatomy of the parotoid gland in Bufonidae with some histochemical findings. I Bufo marinus J Morphol 142:225–239Google Scholar
  52. Hudson CM, Phillips BL, Brown GP, Shine R (2015) Virgins in the vanguard: low reproductive frequency in invasion front cane toads. Biol J Linn Soc 116:743–747CrossRefGoogle Scholar
  53. Hudson CM, Brown GP, Shine R (2016a) It’s lonely at the front: contrasting evolutionary trajectories in male and female invaders. Roy Soc open sci 3:160687CrossRefGoogle Scholar
  54. Hudson CM, Brown GP, Shine R (2016b) Athletic anurans: the impact of morphology, ecology and evolution on climbing ability in invasive cane toads. Biol J Linn Soc 116:743–747CrossRefGoogle Scholar
  55. Jared C, Antoniazzi MM, Jordão AEC, Silva JR, Greven H, Rodrigues MT (2009) Parotoid macroglands in toad (Rhinella jimi): their structure and functioning in passive defense. Toxicon 54:197–207CrossRefPubMedGoogle Scholar
  56. Landová E, Jančúchová-Lásková J, Musilová V, Kadochová S, Frynta D (2013) Ontogenetic switch between alternative antipredatory strategies in the leopard gecko (Eublepharis macularius): defensive threat versus escape. Behav Ecol Sociobiol 67:1113–1122CrossRefGoogle Scholar
  57. Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic & Scientific Publishing, Otley, West Yorkshire, UKGoogle Scholar
  58. Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  59. Magrath RD, Pitcher BJ, Gardner JL (2007) A mutual understanding? Interspecific responses by birds to each other’s aerial alarm calls. Behav Ecol 18:944–951CrossRefGoogle Scholar
  60. Mailho-Fontana PL, Antoniazzi MM, Toledo LF, Verdade VK, Sciani JM, Barbaro KC, Pimenta DC, Rodrigues MT, Jared C (2014) Passive and active defense in toads: the parotoid macroglands in Rhinella marina and Rhaebo guttatus. J Exp Zool 321:65–77CrossRefGoogle Scholar
  61. Mayer M, Shine R, Brown GP (2016) Bigger babies are bolder: effects of body size on personality of hatchling snakes. Behaviour 153:313–323CrossRefGoogle Scholar
  62. McCann S, Greenlees MJ, Newell D, Shine R (2014) Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range. Funct Ecol 28:1166–1174CrossRefGoogle Scholar
  63. Medill SA, Renard A, Lariviére S (2011) Ontogeny of antipredator behavior in striped skunks (Mephitis mephitis). Ethol Ecol Evol 23:41–48CrossRefGoogle Scholar
  64. Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behavior. Proc R Soc Lond B 271:2293–2296CrossRefGoogle Scholar
  65. Natale GS, Alcalde L, Herrera R, Cajade R, Schafer EF, Marangoni F, Trudeau VL (2010) Underwater acoustic communication in the macrophagic carnivorous larvae of Ceratophrys ornata. Acta Zool 92:46–53CrossRefGoogle Scholar
  66. Pennings SC (1990) Predator-prey interactions in opisthobranch gastropods: effects of prey body size and habitat complexity. Mar Ecol-Prog Ser 62:95–101CrossRefGoogle Scholar
  67. Phillips BL, Brown GP, Webb J, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803CrossRefPubMedGoogle Scholar
  68. Phillips BL, Kelehear C, Pizzatto L, Brown GP, Barton D, Shine R (2010) Parasites and pathogens lag behind their host during periods of host range-advance. Ecology 91:872–881CrossRefPubMedGoogle Scholar
  69. Phillips BL, Shine R (2005a) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. P Natl Acad Sci USA 101:17150–17155CrossRefGoogle Scholar
  70. Phillips BL, Shine R (2005b) The morphology, and hence impact, of an invasive species (the cane toad, Bufo marinus) changes with time since colonization. Anim Conserv 8:407–413CrossRefGoogle Scholar
  71. Putman BJ, Coss RG, Clark RW (2015) The ontogeny of antipredator behaviour: age differences in California ground squirrels (Otospermophilus beecheyi) at multiple stages of rattlesnake encounters. Behav Ecol Sociobiol 69:1447–1457CrossRefGoogle Scholar
  72. Rollins LA, Richardson MF, Shine R (2015) A genetic perspective on rapid evolution in cane toads (Rhinella marina). Mol Ecol 24:2264–2276CrossRefPubMedGoogle Scholar
  73. Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210:801–803CrossRefPubMedGoogle Scholar
  74. Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291CrossRefPubMedGoogle Scholar
  75. Shine R, Downes SJ (1999) Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia 119:1–8CrossRefPubMedGoogle Scholar
  76. Shine R, Olsson M, Lemaster MP, Moore IT, Mason RT (2000) Effects of sex, body size, temperature, and location on the anti-predator tactics of free-ranging garter snakes (Thamnophis sirtalis, Colubridae). Behav Ecol 11:239–245CrossRefGoogle Scholar
  77. Shine R, Phillips B, Waye H, Mason RT (2003) Small-scale geographic variation in antipredator tactics of garter snakes. Herpetologica 59:333–339CrossRefGoogle Scholar
  78. Stankowich T (2010) Risk-taking in self-defense. In: Breed MD, Moore J (eds) Encyclopedia of animal behavior, Academic press, vol 3. Oxford, UK, pp 79–86CrossRefGoogle Scholar
  79. Teixeira B, Young J (2014) Can captive-bred American bullfrogs learn to avoid a model avian predator? Acta Ethol 17:15–22CrossRefGoogle Scholar
  80. Tingley R, Greenlees MJ, Shine R (2012) Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959–1965CrossRefGoogle Scholar
  81. Toledo LF, Sazima I, Haddad CFB (2011) Behavioural defences of anurans: an overview. Ethol Ecol Evol 23:1–25CrossRefGoogle Scholar
  82. Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol 111:1–29Google Scholar
  83. Toledo RC, Jared C, Brunner A Jr (1992) Morphology of the large granular alveoli of toad (Bufo ictericus) parotoid glands before and after compression. Toxicon 30:745–753CrossRefPubMedGoogle Scholar
  84. Ward-Fear G, Greenlees MJ, Shine R (2016) Toads on lava: spatial ecology and habitat use of invasive cane toads (Rhinella marina) in Hawai’i. PLoS One 11:e0151700CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wijethunga U, Greenlees MJ, Shine R (2015) The acid test: pH tolerance of the eggs and larvae of the invasive cane toad (Rhinella marina) in southeastern Australia. Physiol Biochem Zool 88:433–443CrossRefPubMedGoogle Scholar
  86. Williams CR, Brodie ED Jr, Tyler MJ, Walker SJ (2000) Antipredator mechanisms of Australian frogs. J Herpetol 34:431–443CrossRefGoogle Scholar
  87. Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LE, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26CrossRefPubMedGoogle Scholar
  88. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249CrossRefGoogle Scholar
  89. Zug GR (1972) Anuran locomotion: structure and function. 1. Preliminary observations on the relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 1972:613–624CrossRefGoogle Scholar
  90. Zug GR (1978) Anuran locomotion—structure and function, 2: jumping performance of semiaquatic, terrestrial, and arboreal frogs. Smithson Contrib Zool 276:1–31CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Life and Environmental Sciences, A08University of SydneyCamperdownAustralia

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