Skip to main content

Cane toads (Rhinella marina) rely on water access, not drought tolerance, to invade xeric Australian environments

Abstract

The invasion of habitats with novel environmental challenges may require physiological tolerances not seen in conspecifics from the native range. We used a combination of field and laboratory-based experiments to assess physiological tolerance to limited water access at four sites distributed across the historical invasion path of cane toads (Rhinella marina) in Australia that, from east to west, alternated between mesic and seasonally xeric habitats. Toads from all locations were well hydrated at the time of capture. However, experimental dehydration caused greater mass loss, higher plasma osmolality, and inhibition of lytic ability in toads from xeric compared to mesic locations. These results suggest somewhat surprisingly that toads from xeric environments are physiologically more vulnerable to water loss. In contrast, bactericidal ability was not sensitive to hydric state and was greater in toads from eastern (long-colonized) areas. Similar patterns in lytic ability in hydrated toads and agglutination ability in wild toads suggest that toads along the invasion front face a tradeoff between enhanced dispersal ability and physiological responses to dehydration. The ability of this invasive species to spread into drier environments may be underpinned by a combination of phenotypic plasticity and evolved (heritable) traits.

This is a preview of subscription content, access via your institution.

Fig. 1

Annual rainfall map for 2016 modified from the Australian Bureau of Meteorology (http://www.bom.gov.au/climate)

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Adams AJ, Kupferberg SJ, Wilber MQ, Pessier AP, Grefsrud M, Bobzien S, Vredenburg VT, Briggs CJ (2017) Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian. Ecosphere 8:e01740. https://doi.org/10.1002/ecs2.1740

    Article  Google Scholar 

  2. Alford RA, Brown GP, Schwarzkopf L, Phillips BL, Shine R (2009) Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species. Wildl Res 36:23. https://doi.org/10.1071/WR08021

    Article  Google Scholar 

  3. Anderson RCO, Bovo RP, Eismann CE, Menegario AA, Andrade DV (2017) Not good, but not all bad: dehydration effects on body fluids, organ masses, and water flux through the skin of Rhinella schneideri (Amphibia, Bufonidae). Physiol Biochem Zool 90:313–320. https://doi.org/10.1086/690189

    Article  PubMed  Google Scholar 

  4. Bartoń K (2015) MuMIn: multi-model inference, R package version 1.15.1. https://CRAN.R-project.org/package=MuMIn. Accessed 1 May 2018

  5. Brown G, Shine R (2014) Immune response varies with rate of dispersal in invasive cane toads (Rhinella marina). PLoS One 9:e99734. https://doi.org/10.1371/journal.pone.0099734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Brown GP, Shilton C, Phillips BL, Shine R (2007) Invasion, stress, and spinal arthritis in cane toads. Proc Natl Acad Sci 104:17698–17700. https://doi.org/10.1073/pnas.0705057104

    Article  PubMed  Google Scholar 

  7. Brown GP, Kelehear C, Shine R (2011) Effects of seasonal aridity on the ecology and behaviour of invasive cane toads in the Australian wet-dry tropics. Funct Ecol 25:1339–1347. https://doi.org/10.1111/j.1365-2435.2011.01888.x

    Article  Google Scholar 

  8. Brown G, Phillis BL, Shine R (2014) The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front. Proc R Soc Lond B Biol Sci 281:20141385. https://doi.org/10.1098/rspb.2014.1385

    Article  Google Scholar 

  9. Brown GP, Kelehear C, Shilton CM, Phillips BL, Shine R (2015a) Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations. Biol J Linn Soc 116:748–760. https://doi.org/10.1111/bij.12623

    Article  Google Scholar 

  10. Brown G, Phillips B, Dubey S, Shine R (2015b) Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia. Ecol Lett 18:57–65. https://doi.org/10.1111/ele.12390

    Article  PubMed  Google Scholar 

  11. Brusch GA, DeNardo DF (2017) When less means more: dehydration improves innate immunity in rattlesnakes. J Exp Biol 220:2287–2295. https://doi.org/10.1242/jeb.155028

    Article  PubMed  Google Scholar 

  12. Brusch GA, Billy G, Blattman JN, DeNardo DF (2017) Reproduction alters hydration state but does not impact the positive effects of dehydration on innate immune function in Children’s pythons (Antaresia childreni). Physiol Biochem Zool 90:646–654. https://doi.org/10.1086/694834

    Article  PubMed  Google Scholar 

  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference a practical information-theoretic approach, 1st edn. Springer Science & Business Media, New York

    Google Scholar 

  14. Chen G, Robert J (2011) Antiviral immunity in amphibians. Viruses 3:2065–2086. https://doi.org/10.3390/v3112065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. 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. https://doi.org/10.1017/S0266467408005695

    Article  Google Scholar 

  16. Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017. https://doi.org/10.1111/mec.13162

    Article  PubMed  Google Scholar 

  17. Cox CL, Cox RM (2015) Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles. Evolution 69:2507–2516. https://doi.org/10.1111/evo.12742

    Article  PubMed  Google Scholar 

  18. Davis JR, DeNardo DF (2009) Water supplementation affects the behavioral and physiological ecology of Gila monsters (Heloderma suspectum) in the Sonoran Desert. Physiol Biochem Zool 82:39–748. https://doi.org/10.1086/605933

    Article  Google Scholar 

  19. de Mendiburu F (2017) Agricolae: statistical procedures for agricultural research, R Package Version, 1.2. https://CRAN.R-project.org/package=agricolae. Accessed 1 May 2018

  20. Devalapalli AP, Lesher A, Shieh K, Solow JS, Everett ML, Edala AS, Whitt P, Long RR, Newton N, Parker W (2006) Increased levels of IgE and autoreactive, polyreactive IgG in wild rodents: implications for the hygiene hypothesis. Scand J Immunol 64:125–136. https://doi.org/10.1111/j.1365-3083.2006.01785.x

    Article  CAS  PubMed  Google Scholar 

  21. Dick JTA, Laverty C, Lennon JJ, Barrios-O’Neill D, Mensink PJ, Britton RJ, Medoc V, Boets P, Alexander ME, Taylor NG, Dunn AM, Hatcher MJ, Rosewarne PJ, Crookes S, Maclsaac HJ, Xu M, Ricciardi A, Wasserman RJ, Ellender BR, Weyl OLF, Lucy FE, Banks PB, Dodd JA, MacNeil C, Penk MR, Aldridge DC, Caffrey JM (2017) Invader relative impact potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. J Appl Ecol 54:1259–1267. https://doi.org/10.1111/1365-2664.12849

    Article  Google Scholar 

  22. Dmi’el R (2001) Skin resistance to evaporative water loss in reptiles: a physiological adaptive mechanism to environmental stress or a phyletically dictated trait? Isr J Zool 47:55–67. https://doi.org/10.1560/ENQ9-KD7R-WFGW-KUQW

    Article  Google Scholar 

  23. Donohue I, Petchey OL, Montoya JM, Jackson AL, Mcnally L, Viana M, Healy K, Lurgi M, O’Connor NE, Emmerson MC (2013) On the dimensionality of ecological stability. Ecol Lett 16:421–429. https://doi.org/10.1111/ele.12086

    Article  PubMed  Google Scholar 

  24. Freidenreich DJ, Volek JS (2013) The immune response to exercise: effects on cellular mobilization, immune function and muscle regeneration. In: Bagchi D, Nair S, Sen CK (eds) Nutrition and enhanced sports performance: muscle building, endurance, and strength. Academic Press, Cambridge, pp 95–101

    Chapter  Google Scholar 

  25. French SS, Neuman-Lee LA (2012) Improved ex vivo method for microbiocidal activity across vertebrate species. Biol Open 1:482–487. https://doi.org/10.1242/bio.2012919

    Article  PubMed Central  PubMed  Google Scholar 

  26. Goetz SM, Romagosa CM, Appel AG, Guyer C, Mendonça MT (2017) Reduced innate immunity of Cuban tree frogs at leading edge of range expansion. J Exp Zool A Ecol Integr Physiol 327:592–599. https://doi.org/10.1002/jez.2146

    CAS  Article  PubMed  Google Scholar 

  27. 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. https://doi.org/10.1371/journal.pone.0049351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Gruber J, BrownG Whiting MJ, Shine R (2017) Is the behavioural divergence between range-core and range-edge populations of cane toads (Rhinella marina) due to evolutionary change or developmental plasticity? R Soc Open Sci 4:170789. https://doi.org/10.1098/rsos.170789

    Article  PubMed Central  PubMed  Google Scholar 

  29. Hendry AP (2015) Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J Hered 107:25–41. https://doi.org/10.1093/jhered/esv060

    Article  PubMed  Google Scholar 

  30. Hillman SS (1980) Physiological correlates of differential dehydration tolerance in anuran amphibians. Copeia 1980:125–129

    Article  Google Scholar 

  31. Hillyard SD, Hoff KS, Propper C (1998) The water absorption response: a behavioral assay for physiological processes in terrestrial amphibians. Physiol Zool 71:127–138. https://doi.org/10.1086/515900

    Article  CAS  PubMed  Google Scholar 

  32. Hoang A (2007) Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55:2353–2358. https://doi.org/10.1111/j.0014-3820.2001.tb00748.x

    Article  Google Scholar 

  33. Hudson CM, McCurry MR, Lundgren P, McHenry CR, Shine R (2016) Constructing an invasion machine: the rapid evolution of a dispersal-enhancing phenotype during the cane toad invasion of Australia. PLoS One 11:e0156950. https://doi.org/10.1371/journal.pone.0156950

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1111/j.2008.0906-7590-05457.x

    Article  Google Scholar 

  35. Kiesecker JM, Skelly DK (2001) Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology 82:1956–1963. https://doi.org/10.1890/0012-9658(2001)082%5b1956:EODAPD%5d2.0.CO;2

    Article  Google Scholar 

  36. Kilvitis HJ, Hanson H, Schrey AW, Martin LB (2017) Epigenetic potential as a mechanism of phenotypic plasticity in vertebrate range expansions. Integr Comp Biol 57:385–395. https://doi.org/10.1093/icb/icx082

    Article  CAS  PubMed  Google Scholar 

  37. Kosmala GK, Brown GP, Christian KA, Hudson CM, Shine R (2018) The thermal dependency of locomotor performance evolves rapidly within an invasive species. Ecol Evol 8:4403–4408. https://doi.org/10.1002/ece3.3996

    Article  PubMed Central  PubMed  Google Scholar 

  38. Laverty C, Brenner D, McIlwaine C, Lennon JJ, Dick JTA, Lucy FE, Christian KA (2017) Temperature rise and parasitic infection interact to increase the impact of an invasive species. Int J Parasitol 47:291–296. https://doi.org/10.1016/j.ijpara.2016.12.004

    Article  PubMed  Google Scholar 

  39. Lever C (2001) The cane toad: the history and ecology of a successful colonist, 1st edn. Westbury Academic & Scientific Publishing, Otley

    Google Scholar 

  40. Lindstrom T, Brown GP, Sisson SA, Phillips BL, Shine R (2013) Rapid shifts in dispersal behavior on an expanding range edge. Proc Natl Acad Sci 110:13452–13456. https://doi.org/10.1073/pnas.1303157110

    Article  PubMed  Google Scholar 

  41. Llewellyn D, Brown GP, Thompson MB, Shine R (2011) Behavioral responses to immune-system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies. Physiol Biochem Zool 84:77–86. https://doi.org/10.1086/657609

    Article  CAS  PubMed  Google Scholar 

  42. Martin LB, Kilvitis HJ, Brace AJ, Cooper L, Haussmann MF, Mutati A, Fasanello V, O’Brien S, Ardia DR (2017) Costs of immunity and their role in the range expansion of the house sparrow in Kenya. J Exp Biol 220:2228–2235. https://doi.org/10.1242/jeb.154716

    Article  PubMed  Google Scholar 

  43. Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286. https://doi.org/10.1016/j.dci.2004.07.006

    Article  CAS  PubMed  Google Scholar 

  44. 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 28:1166–1174. https://doi.org/10.1111/1365-2435.12255

    Article  Google Scholar 

  45. McCann SM, Kosmala GK, Greenlees MJ, Shine R (2018) Physiological plasticity in a successful invader: rapid acclimation to cold occurs only in cool-climate populations of cane toads (Rhinella marina). Cons Physiol 6:cox072. https://doi.org/10.1093/conphys/cox072

    Article  Google Scholar 

  46. Mery F, Burns JG (2010) Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24:571–583. https://doi.org/10.1007/s10682-009-9336-y

    Article  Google Scholar 

  47. Moeller KT, Butler MW, DeNardo DF (2013) The effect of hydration state and energy balance on innate immunity of a desert reptile. Front Zool 10:23. https://doi.org/10.1186/1742-9994-10-23

    Article  PubMed Central  PubMed  Google Scholar 

  48. Montecino-Rodriguez E, Berent-Maoz B, Dorshkind K (2013) Causes, consequences, and reversal of immune system aging. J Clin Investig 123:958–965. https://doi.org/10.1172/JCI64096

    Article  CAS  PubMed  Google Scholar 

  49. Muñoz-Garcia A, Larraín P, Ben-Hamo M, Cruz-Neto A, Williams JB, Pinshow B, Korine C (2016) Metabolic rate, evaporative water loss and thermoregulatory state in four species of bats in the Negev desert. Comp Biochem Physiol A Mol Integr Physiol 191:156–165. https://doi.org/10.1016/j.cbpa.2015.10.010

    Article  CAS  PubMed  Google Scholar 

  50. Myles-Gonzalez E, Burness G, Yavno S, Rooke A, Fox MG (2015) To boldly go where no goby has gone before: boldness, dispersal tendency, and metabolism at the invasion front. Behav Ecol 26:1083–1090. https://doi.org/10.1093/beheco/arv050

    Article  Google Scholar 

  51. Peneaux C, Machovsky-Capuska GE, Raubenheimer D, Lermite F, Rousseau C, Ruhan T, Rodger JC, Griffin AS (2017) Tasting novel foods and selecting nutrient content in a highly successful ecological invader, the common myna. J Avian Biol 48:1432–1440. https://doi.org/10.1111/jav.01456

    Article  Google Scholar 

  52. Perkins TA, Phillips BL, Baskett ML, Hastings A (2013) Evolution of dispersal and life history interact to drive accelerating spread of an invasive species. Ecol Lett 16:1079–1087. https://doi.org/10.1111/ele.12136

    Article  PubMed  Google Scholar 

  53. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803. https://doi.org/10.1038/439803a

    Article  CAS  PubMed  Google Scholar 

  54. 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. https://doi.org/10.1111/j.1442-9993.2007.01664.x

    Article  Google Scholar 

  55. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: linear and nonlinear mixed effects models. R package version 3.1-137. https://CRAN.R-project.org/package=nlme

  56. Pizzatto L, Kelehear C, Shine R (2013) Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala, in recently colonised cane toad (Rhinella marina) populations in tropical Australia. Int J Parasitol 43:753–761. https://doi.org/10.1016/j.ijpara.2013.05.002

    Article  PubMed  Google Scholar 

  57. Pizzatto L, Both C, Shine R (2014) Quantifying anuran microhabitat use to infer the potential for parasite transmission between invasive cane toads and two species of Australian native frogs. PLoS One 9:e106996. https://doi.org/10.1371/journal.pone.0106996

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Prates I, Navas CA (2009) Cutaneous resistance to evaporative water loss in Brazilian Rhinella (Anura: Bufonidae) from contrasting environments. Copeia 2009:618–622. https://doi.org/10.1643/CP-08-128

    Article  Google Scholar 

  59. Prates I, Angilleta MJ, Wilson RS, Niehaus AC, Navas CA (2013) Dehydration hardly slows hopping toads (Rhinella granulosa) from xeric and mesic environments. Physiol Biochem Zool 86:451–457. https://doi.org/10.1086/671191

    Article  PubMed  Google Scholar 

  60. Ramsay DJ, Thrasher TN (1984) The defence of plasma osmolality. J Physiol (Paris) 79:416–420

    CAS  Google Scholar 

  61. Reisinger LS, Elgin AK, Towle KM, Chan DJ, Lodge DM (2017) The influence of evolution and plasticity on the behavior of an invasive crayfish. Biol Invasions 19:815–830. https://doi.org/10.1007/s10530-016-1346-4

    Article  Google Scholar 

  62. Reynolds SJ, Christian KA (2009) Environmental moisture availability and body fluid osmolality in introduced toads, Rhinella marina, in monsoonal northern Australia. J Herpetol 43:326–331. https://doi.org/10.1670/08-062R2.1

    Article  Google Scholar 

  63. Rollins LA, Richardson MF, Shine R (2015) A genetic perspective on rapid evolution in cane toads (Rhinella marina). Mol Ecol 24:2264–2276. https://doi.org/10.1111/mec.13184

    Article  PubMed  Google Scholar 

  64. Schwarzkopf L, Alford RA (1996) Desiccation and shelter-site use in a tropical amphibian: comparing toads with physical models. Funct Ecol 10:193–200. https://doi.org/10.2307/2389843

    Article  Google Scholar 

  65. 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. https://doi.org/10.2307/1565716

    Article  Google Scholar 

  66. Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436. https://doi.org/10.1146/annurev.ecolsys.110308.120317

    Article  Google Scholar 

  67. Shilton CM, Brown GP, Benedict S, Shine R (2008) Spinal arthropathy associated with Ochrobactrum anthropi in free-ranging cane toads (Chaunus [Bufo] marinus) in Australia. Vet Pathol 45:85–94. https://doi.org/10.1354/vp.45-1-85

    Article  CAS  PubMed  Google Scholar 

  68. Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291. https://doi.org/10.1086/655116

    Article  PubMed  Google Scholar 

  69. Shine R (2012) Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol Appl 5:107–116. https://doi.org/10.1111/j.1752-4571.2011.00201.x

    Article  PubMed  Google Scholar 

  70. Shine R, Brown GP (2008) Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics. Philos Trans R Soc B Biol Sci 363:363–373. https://doi.org/10.1098/rstb.2007.2144

    Article  Google Scholar 

  71. Silva-Rocha I, Salvi D, Sillero N, Mateo JA, Carretero MA (2015) Snakes on the balearic islands: an invasion tale with implications for native biodiversity conservation. PLoS One 10:e0121026. https://doi.org/10.1371/journal.pone.0121026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, Garcia-Berthou E, Pascal M, Pysek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013

    Article  Google Scholar 

  73. Stockham S, Scott M (2013) Fundamentals of veterinary clinical pathology, 1st edn. Wiley, Hoboken

    Google Scholar 

  74. Sutherst RW, Floyd RB, Maywald GF (1996) The potential geographical distribution of the cane toad, Bufo marinus L. in Australia. Cons Biol 1:294–299. https://doi.org/10.1046/j.1523-1739.1996.10010294.x

    Article  Google Scholar 

  75. 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. https://doi.org/10.1371/journal.pone.0025979

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. 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. https://doi.org/10.1111/j.1600-0706.2012.20422.x

    Article  Google Scholar 

  77. Tingley R, Vallinoto M, Sequeira F, Kearney MR (2014) Realized niche shift during a global biological invasion. Proc Natl Acad Sci 111:10233–10238. https://doi.org/10.1073/pnas.1405766111

    Article  CAS  PubMed  Google Scholar 

  78. 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 B Biol Sci 274:1413–1419. https://doi.org/10.1098/rspb.2007.0114

    Article  Google Scholar 

  79. 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. https://doi.org/10.1086/527494

    Article  PubMed  Google Scholar 

  80. Warfe DM, Pettit NE, Davies PM, Pusey BJ, Hamilton SK, Kennard MJ, Townsend SA, Bayliss P, Ward DP, Douglas MM, Burford MA, Finn M, Bunn SE, Halliday IA (2011) The “wet-dry” in the wet-dry tropics drives river ecosystem structure and processes in northern Australia. Freshw Biol 56:2169–2195. https://doi.org/10.1111/j.1365-2427.2011.02660.x

    Article  Google Scholar 

  81. Webb JK, Letnic M, Jessop TS, Dempster T (2014) Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment. Biol Lett 10:20131014. https://doi.org/10.1098/rsbl.2013.1014

    Article  PubMed Central  PubMed  Google Scholar 

  82. Wright TF, Eberhard JR, Hobson EA, Avery ML, Russello MA (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22:393–404. https://doi.org/10.1080/03949370.2010.505580

    Article  Google Scholar 

  83. Young JE, Christian KA, Donnellan S, Tracy CR, Parry D (2005) Comparative analysis of cutaneous evaporative water loss in frogs demonstrates correlation with ecological habits. Physiol Biochem Zool 78:847–856. https://doi.org/10.1086/432152

    Article  PubMed  Google Scholar 

  84. Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resumé of native populations. Smithson Contrib Zool 1979:1–58. https://doi.org/10.5479/si.00810282.284

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank all members of the Shine lab at Middle Point, the staff at the Australian Academy of Sciences (especially S. Owen), and faculty and staff at Charles Darwin University for their assistance. GABIV wishes to particularly thank the Christian-Gibb family for their generosity. Finally, we wish to thank Drs. M. Greenlees, K. Gibb, and M. Angilletta for their contributions. This work was supported by the National Science Foundation Graduate Research Fellowship, Directorate for Biological Sciences (Grant #1311230), National Science Foundation East Asia and Pacific Summer Institute Fellowship, Directorate for Biological Sciences (Grant #1606367), and Arizona State University’s College of Liberal Arts & Sciences Graduate Excellence Fellowship for First-Generation Students for GABIV.

Author information

Affiliations

Authors

Contributions

GABIV, KC, GPB, RS and DD designed the study. GABIV and KC conducted the field work. GABIV conducted all assays, performed the statistical analyses, and led the writing of the manuscript. DD, KC, GPB, and RS contributed to revisions and gave final approval for publication.

Corresponding author

Correspondence to George A. Brusch IV.

Ethics declarations

Data accessibility

The datasets supporting this article can be accessed at https://doi.org/10.6084/m9.figshare.6431108.

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by Indrikis Krams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 369 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Brusch, G.A., Christian, K., Brown, G.P. et al. Cane toads (Rhinella marina) rely on water access, not drought tolerance, to invade xeric Australian environments. Oecologia 189, 307–316 (2019). https://doi.org/10.1007/s00442-018-4321-1

Download citation

Keywords

  • Bufo marinus
  • Hydroregulation
  • Innate immunity
  • Invasive species
  • Osmolality