Cane toads (Rhinella marina) rely on water access, not drought tolerance, to invade xeric Australian environments
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.
KeywordsBufo marinus Hydroregulation Innate immunity Invasive species Osmolality
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 contribution statement
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.
Compliance with ethical standards
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.
- 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 CrossRefPubMedGoogle Scholar
- Bartoń K (2015) MuMIn: multi-model inference, R package version 1.15.1. https://CRAN.R-project.org/package=MuMIn. Accessed 1 May 2018
- 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 CrossRefPubMedGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference a practical information-theoretic approach, 1st edn. Springer Science & Business Media, New YorkGoogle Scholar
- 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
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 95–101CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefGoogle Scholar
- Lever C (2001) The cane toad: the history and ecology of a successful colonist, 1st edn. Westbury Academic & Scientific Publishing, OtleyGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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
- Ramsay DJ, Thrasher TN (1984) The defence of plasma osmolality. J Physiol (Paris) 79:416–420Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Stockham S, Scott M (2013) Fundamentals of veterinary clinical pathology, 1st edn. Wiley, HobokenGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar