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The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments?

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Abstract

Invasive species must respond appropriately to novel habitats as they expand their ranges. The degree of habitat novelty is likely to be the highest immediately following human-mediated range-expansion, which can move an individual very large distances beyond its home range within a short space of time. How does translocation affect those critically important initial colonists? We collected cane toads (Rhinella marina) in eastern Australia in heath and woodland habitats, simulated either short-distance or long-distance transport (level of transport stress) and then either returned toads to their exact collection point or reciprocally translocated them to a novel site. Following release, we radio-tracked toads for 5 days and recorded their shelter types and microhabitat use daily. We also examined the thermal and hydric conditions experienced by toads and tested if prey intake, stomach mass and body condition of translocated toads differed from those of resident conspecifics. Translocated toads used different types of diurnal shelters, were more exposed by day and experienced higher diurnal temperatures (but not more desiccating conditions). Analysis of stomach contents indicated that translocation per se did not reduce feeding rates, nor reduce body condition. However, toads exposed to higher transport stress (simulating long-distance displacement) exhibited changes to body condition and hydric balance. Shifts in toad shelter site use induced by translocation may increase the toads’ visibility to diurnal predators, thereby reducing toad survival but also exacerbating the ecological impact of toads during the initial phase of post-translocation dispersal.

Significance statement

Each stage of the invasion process poses unique challenges for invading taxa, and very few species possess the full suite of behavioural, physiological or morphological traits required to pass through all stages of the invasion pathway. Although the study of invasion biology has grown exponentially, most research has focused on the determinants of invasion success during the later stages of establishment and spread, neglecting the earlier stages of transport and introduction. Understanding how species respond to all stages of the invasion process can clarify the non-random traits that allow certain species to become successful invaders.

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References

  • Amiel JJ, Tingley R, Shine R (2011) Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One 6:e18277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackburn TM, Duncan RP (2001) Establishment patterns of exotic birds are constrained by non-random patterns in introduction. J Biogeogr 28:927–939

    Article  Google Scholar 

  • Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  PubMed  Google Scholar 

  • Boland CRJ (2004) Introduced cane toads Bufo marinus are active nest predators and competitors of rainbow bee-eaters Merops ornatus: observational and experimental evidence. Biol Conserv 120:53–62

    Article  Google Scholar 

  • Chapple DG, Knegtmans J, Kikillus H, van Winkel D (2016) Biosecurity of exotic reptiles and amphibians in New Zealand: building upon Tony Whitaker's legacy. J Roy Soc New Zeal 46:66–84

    Article  Google Scholar 

  • Chapple DG, Simmonds SM, Wong B (2011) Know when to run, know when to hide: can behavioral differences explain the divergent invasion success of two sympatric lizards? Ecol Evol 1:278–289

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapple DG, Simmonds SM, Wong BBM (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27:57–64

    Article  PubMed  Google Scholar 

  • Child T, Phillips BL, Shine R (2009) Does desiccation risk drive the distribution of juvenile cane toads (Bufo marinus) in tropical Australia? J Trop Ecol 25:193–200

    Article  Google Scholar 

  • Coggan N, Clissold FJ, Simpson SJ (2011) Locusts use dynamic thermoregulatory behaviour to optimize nutritional outcomes. Proc R Soc Lond B 278:2745–2752

    Article  Google Scholar 

  • Cohen MP, Alford RA (1996) Factors affecting diurnal shelter use by the cane toad, Bufo marinus. Herpetologica 52:172–181

    Google Scholar 

  • Dallman MF, Pecoraro N, Akana SF et al (2003) Chronic stress and obesity: a new view of “comfort food”. P Natl Acad Sci USA 100:11696–11701

    Article  CAS  Google Scholar 

  • Dickens MJ, Delehanty DJ, Michael Romero L (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341

    Article  Google Scholar 

  • Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606

    Article  Google Scholar 

  • Gerber L, Seabloom E, Burton R, Reichman O (2003) Translocation of an imperilled woodrat population: integrating spatial and habitat patterns. Anim Conserv 6:309–316

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  PubMed  Google Scholar 

  • Gilroy JJ, Sutherland WJ (2007) Beyond ecological traps: perceptual errors and undervalued resources. Trends Ecol Evol 22:351–356

    Article  PubMed  Google Scholar 

  • González-Bernal E, Greenlees M, Brown GP, Shine R (2012) Cane toads on cowpats: commercial livestock production facilitates toad invasion in tropical Australia. PLoS One 7:e49351

  • González-Bernal E, Greenlees MJ, Brown GP, Shine R (2016) Toads in the backyard: why do invasive cane toads (Rhinella marina) prefer buildings to bushland? Popul Ecol 58:293–302

  • Gosler AG (1996) Environmental and social determinants of winter fat storage in the great tit Parus major. J Anim Ecol 65:1–17

    Article  Google Scholar 

  • Griffin AS, Blumstein DT, Evans CS (2000) Training captive-bred or translocated animals to avoid predators. Conserv Biol 14:1317–1326

    Article  Google Scholar 

  • Griffiths AD, McKay JL (2008) Cane toads reduce the abundance and site occupancy of Merten's water monitor (Varanus mertensi). Wildlife Res 34:609–615

    Article  Google Scholar 

  • Holding ML, Owen DAS, Taylor EN (2014) Evaluating the thermal effects of translocation in a large-bodied pitviper. J Exp Zool A 321:442–449

    Article  Google Scholar 

  • Hsu J (1996) Multiple comparisons: theory and methods. CRC Press, Boca Raton

    Book  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Jessop TS, Letnic M, Webb JK, Dempster T (2013) Adrenocortical stress responses influence an invasive vertebrate's fitness in an extreme environment. Proc R Soc B 280:20131444

    Article  PubMed  PubMed Central  Google Scholar 

  • Jolly CJ, Shine R, Greenlees MJ (2015) The impact of invasive cane toads on native wildlife in southern Australia. Ecol Evol 5:3879–3894

    Article  PubMed  PubMed Central  Google Scholar 

  • Kearney M, Phillips BL, Tracy CR, Christian KA, Betts G, Porter WP (2008) Modelling species distributions without using species distributions: the cane toad in Australia under current and future climates. Ecography 31:423–434

    Article  Google Scholar 

  • Letnic M, Webb JK, Shine R (2008) Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia. Biol Conserv 141:1773–1782

    Article  Google Scholar 

  • Lever C (2001) The cane toad: the history and ecology of a successful colonist. Westbury Academic & Scientific Publishing, Otley, West Yorkshire

    Google Scholar 

  • Lockwood JL (1999) Using taxonomy to predict success among introduced avifauna: relative importance of transport and establishment. Conserv Biol 13:560–567

    Article  Google Scholar 

  • Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Malvin GM, Wood SC (1991) Behavioral thermoregulation of the toad, Bufo marinus: effects of air humidity. J Exp Zool 258:322–326

    Article  CAS  PubMed  Google Scholar 

  • McDonald RC, Isbell R, Speight JG, Walker J, Hopkins M (1998) Australian soil and land survey: field handbook, 2nd edn. CSIRO publishing, Collingwood, Australia

    Google Scholar 

  • Medley KA, Jenkins DG, Hoffman EA (2015) Human-aided and natural dispersal drive gene flow across the range of an invasive mosquito. Mol Ecol 24:284–295

    Article  PubMed  Google Scholar 

  • Narayan EJ, Hero JM (2014) Acute thermal stressor increases glucocorticoid response but minimizes testosterone and locomotor performance in the cane toad (Rhinella marina). PLoS One 9:e92090

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell S, Webb JK, Shine R (2010) Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader. J Appl Ecol 47:558–565

    Article  Google Scholar 

  • Pettit (2016) Responses of an invader to the early stages of the invasion pathway. Honours Thesis, School of Life and Environmental Sciences, University of Sydney, Australia

  • Philibert A, Desprez-Loustau M, Fabre B et al (2011) Predicting invasion success of forest pathogenic fungi from species traits. J Appl Ecol 48:1381–1390

    Article  Google Scholar 

  • Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747

    Article  Google Scholar 

  • Price-Rees SJ, Brown GP, Shine R (2010) Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia. Wildlife Res 37:166–173

    Article  Google Scholar 

  • Richards S, Sinsch U, Alford R (1994) Radio tracking. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MC (eds) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington, DC, pp. 155–157

    Google Scholar 

  • Roznik EA, Alford RA (2012) Does waterproofing thermochron iButton dataloggers influence temperature readings? J Therm Biol 37:260–264

    Article  Google Scholar 

  • Schwarzkopf L, Alford RA (1996) Desiccation and shelter-site use in a tropical amphibian: comparing toads with physical models. Funct Ecol 10:193–200

    Article  Google Scholar 

  • Seebacher F, Alford RA (1999) Movement and microhabitat use of a terrestrial amphibian (Bufo marinus) on a tropical island: seasonal variation and environmental correlates. J Herpetol 33:208–214

    Article  Google Scholar 

  • Seebacher F, Alford RA (2002) Shelter microhabitats determine body temperature and dehydration rates of a terrestrial amphibian (Bufo marinus). J Herpetol 36:69–75

    Article  Google Scholar 

  • Shine BR (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291

    Article  PubMed  Google Scholar 

  • Shine R, Amiel J, Munn AJ, Stewart M, Vyssotski AL, Lesku JA (2015) Is “cooling then freezing” a humane way to kill amphibians and reptiles? Biol Open 4:760–763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slagsvold T, Dale S, Kruszewicz A (1995) Predation favours cryptic coloration in breeding male pied flycatchers. Anim Behav 50:1109–1121

    Article  Google Scholar 

  • Smith J, Phillips B (2006) Toxic tucker: the potential impact of cane toads on Australian reptiles. Pacific Conserv Biol 12:40–49

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman, New York

    Google Scholar 

  • Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. P Natl Acad Sci USA 102:5460–5465

    Article  CAS  Google Scholar 

  • Somers MJ, Graf JA, Szykman M, Slotow R, Gusset M (2008) Dynamics of a small re-introduced population of wild dogs over 25 years: Allee effects and the implications of sociality for endangered species’ recovery. Oecologia 158:239–247

    Article  PubMed  Google Scholar 

  • Tingley R, Greenlees MJ, Shine R (2012) Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959–1965

    Article  Google Scholar 

  • Tingley R, Romagosa CM, Kraus F, Bickford D, Phillips BL, Shine R (2010) The frog filter: amphibian introduction bias driven by taxonomy, body size and biogeography. Glob Ecol Biogeogr 19:496–503

    Google Scholar 

  • Tingley R, Shine R (2011) Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the Australian semi-desert. PLoS One 6:e25979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 B 274:1413–1419

    Article  Google Scholar 

  • Urban MC, Phillips BL, Skelly DK, Shine R (2008) A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia. Am Nat 171:E134–E148

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010a) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010b) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Ward-Fear G, Brown GP, Shine R (2010) Using a native predator (the meat ant, Iridomyrmex reburrus) to reduce the abundance of an invasive species (the cane toad, Bufo marinus) in tropical Australia. J Appl Ecol 47:273–280

    Article  Google Scholar 

  • White AW, Shine R (2009) The extra-limital spread of an invasive species via ‘stowaway’ dispersal: toad to nowhere? Anim Conserv 12:38–45

    Article  Google Scholar 

  • Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666

    Article  Google Scholar 

  • Wygoda ML (1984) Low cutaneous evaporative water loss in arboreal frogs. Physiol Zool 57:329–337

    Article  Google Scholar 

  • Yoder JM (2004) The cost of dispersal: predation as a function of movement and site familiarity in ruffed grouse. Behav Ecol 15:469–476

    Article  Google Scholar 

  • Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithsonian Institution Press, Washington, DC

    Google Scholar 

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Acknowledgements

We thank Renee Silvester for assistance in the field and Melanie Elphick for helping prepare this manuscript. We also thank the reviewers for their constructive comments.

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Authors and Affiliations

  1. School of Life and Environmental Sciences, University of Sydney, NSW, 2006, Australia

    Lachlan J. Pettit, Matthew J. Greenlees & Richard Shine

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  1. Lachlan J. Pettit
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  2. Matthew J. Greenlees
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  3. Richard Shine
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Correspondence to Richard Shine.

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Ethical statement

All applicable international, national and institutional guidelines for the care and use of animals were followed (University of Sydney Animal Ethics Committee Protocol 2015/853).

Funding

The work was funded by the Australian Research Council (FL120100074).

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The authors declare that they have no competing interests.

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Communicated by D W. Pfennig

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Pettit, L.J., Greenlees, M.J. & Shine, R. The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments?. Behav Ecol Sociobiol 71, 15 (2017). https://doi.org/10.1007/s00265-016-2245-5

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