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Oecologia

, Volume 184, Issue 2, pp 411–422 | Cite as

The impact of transportation and translocation on dispersal behaviour in the invasive cane toad

  • Lachlan Pettit
  • Matthew Greenlees
  • Richard Shine
Behavioral ecology – original research

Abstract

Biological invasions transport organisms to novel environments; but how does the translocation process influence movement patterns of the invader? Plausibly, the stress of encountering a novel environment, or of the transport process, might induce rapid dispersal from the release site—potentially enhancing (or reducing) invader success and spread. We investigated the effect of transportation and release to novel environments on dispersal-relevant traits of one of the world’s most notorious invaders, the cane toad (Rhinella marina). We collected toads in northern New South Wales from heath and woodland habitats, manipulated the level of transport stress and either returned toads to their exact collection point (residents) or reciprocally translocated them to a novel site. Both translocation and the level of transport stress drastically altered toad dispersal rates for at least 5 days post-release. Translocated toads (depending on their level of transport stress and release habitat) moved on average two to five times further per day (mean range 67–148 m) than did residents (mean range 22–34 m). Translocated toads also moved on more days, and moved further from their release point than did resident toads, but did not move in straighter lines. A higher level of transport stress (simulating long-distance translocation) had no significant effect on movements of resident toads but amplified the dispersal of translocated toads only when released into woodland habitat. These behavioural shifts induced by translocation and transportation may affect an invader’s ability to colonise novel sites, and need to be incorporated into plans for invader control.

Keywords

Alien species Translocation Bufo marinus Dispersal Invasion 

Notes

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. Funding was provided by the Australian Research Council (FL120100074).

Author contribution statement

LP helped design the study, collected field data, conducted statistical analyses and drafted the manuscript. RS and MG conceived, designed and coordinated the study and helped draft the manuscript. All authors gave approval for publication.

Supplementary material

442_2017_3871_MOESM1_ESM.pdf (551 kb)
Supplementary material 1 (PDF 551 kb)

References

  1. 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 36:23–28. doi: 10.1071/WR08021 CrossRefGoogle Scholar
  2. 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. doi: 10.1371/journal.pone.0018277 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Attum O, Cutshall CD (2015) Movement of translocated turtles according to translocation method and habitat structure. Restor Ecol 23:588–594. doi: 10.1111/rec.12233 CrossRefGoogle Scholar
  4. Attum O, Otoum M, Amr Z, Tietjen B (2011) Movement patterns and habitat use of soft-released translocated spur-thighed tortoises, Testudo graeca. Eur J Wildl Res 57:251–258. doi: 10.1007/s10344-010-0419-4 CrossRefGoogle Scholar
  5. Batschelet E (1981) Circular statistics in biology. Academic Press, LondonGoogle Scholar
  6. Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JR, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. doi: 10.1016/j.tree.2011.03.023 CrossRefPubMedGoogle Scholar
  7. Bleach IT, Beckmann C, Both C, Brown GP, Shine R (2015) Noisy neighbours at the frog pond: effects of invasive cane toads on the calling behaviour of native Australian frogs. Behav Ecol Sociobiol 69:675–683. doi: 10.1007/s00265-015-1879-z CrossRefGoogle Scholar
  8. 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. doi: 10.1016/j.biocon.2004.01.025 CrossRefGoogle Scholar
  9. Brown GP, Phillips BL, Webb JK, Shine R (2006) Toad on the road: use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biol Conserv 133:88–94. doi: 10.1016/j.biocon.2006.05.020 CrossRefGoogle Scholar
  10. Bureau of Meteorology (2016) Climate data online. http://www.bom.gov.au/climate/data/. Accessed Jan 2016
  11. 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 R Soc NZ 46:66–84. doi: 10.1080/03036758.2015.1108344 CrossRefGoogle Scholar
  12. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. doi: 10.1016/j.tree.2005.01.003 CrossRefPubMedGoogle Scholar
  13. Dana ED, Jeschke JM, García-de-Lomas J (2013) Decision tools for managing biological invasions: existing biases and future needs. Oryx 48:56–63. doi: 10.1017/s0030605312001263 CrossRefGoogle Scholar
  14. Davis MA (2003) Biotic globalization: does competition from introduced species threaten biodiversity? Bioscience 53:481–489. doi: 10.1641/0006-3568 CrossRefGoogle Scholar
  15. Dickens MJ, Delehanty DJ, Romero LM (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341. doi: 10.1016/j.biocon.2010.02.032 CrossRefGoogle Scholar
  16. Florance D, Webb JK, Dempster T, Kearney MR, Worthing A, Letnic M (2011) Excluding access to invasion hubs can contain the spread of an invasive vertebrate. Proc R Soc Lond B Biol Sci 278:2900–2908. doi: 10.1098/rspb.2011.0032 CrossRefGoogle Scholar
  17. Gilroy JJ, Sutherland WJ (2007) Beyond ecological traps: perceptual errors and undervalued resources. Trends Ecol Evol 22:351–356. doi: 10.1016/j.tree.2007.03.014 CrossRefPubMedGoogle Scholar
  18. González-Bernal E, Brown GP, Cabrera-Guzmán E, Shine R (2011) Foraging tactics of an ambush predator: the effects of substrate attributes on prey availability and predator feeding success. Behav Ecol Sociobiol 65:1367–1375. doi: 10.1007/s00265-011-1147-9 CrossRefGoogle Scholar
  19. Graham SP, Kelehear C, Brown GP, Shine R (2012) Corticosterone-immune interactions during captive stress in invading Australian cane toads (Rhinella marina). Horm Behav 62:146–153. doi: 10.1016/j.yhbeh.2012.06.001 CrossRefPubMedGoogle Scholar
  20. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474. doi: 10.1016/j.tree.2004.07.005 CrossRefPubMedGoogle Scholar
  21. Hoffmann G (1983) The search behavior of the desert isopod Hemilepistus reaumuri as compared with a systematic search. Behav Ecol Sociobiol 13:93–106. doi: 10.1007/BF00293799 CrossRefGoogle Scholar
  22. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18. doi: 10.1111/j.1365-2664.2008.01600.x CrossRefGoogle Scholar
  23. 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 Lond B Biol Sci 280:20131444. doi: 10.1098/rspb.2013.1444 CrossRefGoogle Scholar
  24. Jolly CJ, Shine R, Greenlees MJ (2015) The impact of invasive cane toads on native wildlife in southern Australia. Ecol Evol 5:3879–3894. doi: 10.1002/ece3.1657 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204. doi: 10.1016/S0169-5347(01)02101-2 CrossRefPubMedGoogle Scholar
  26. Kolbe JJ, Kearney M, Shine R (2010) Modeling the consequences of thermal trait variation for the cane toad invasion of Australia. Ecol Appl 20:2273–2285CrossRefPubMedGoogle Scholar
  27. Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic and Scientific Publishing, OtleyGoogle Scholar
  28. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi: 10.1016/j.tree.2005.02.004 CrossRefPubMedGoogle Scholar
  29. Marable MK, Belant JL, Godwin D, Wang G (2012) Effects of resource dispersion and site familiarity on movements of translocated wild turkeys on fragmented landscapes. Behav Processes 91:119–124. doi: 10.1016/j.beproc.2012.06.006 CrossRefPubMedGoogle Scholar
  30. 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. doi: 10.1111/1365-2435.12255 CrossRefGoogle Scholar
  31. Miller K (1982) Effect of temperature on sprint performance in the frog Xenopus laevis and the salamander Necturus maculosus. Copeia 1982:695–698. doi: 10.2307/1444671 CrossRefGoogle Scholar
  32. Narayan EJ, Cockrem JF, Hero JM (2011) Urinary corticosterone metabolite responses to capture and captivity in the cane toad (Rhinella marina). Gen Comp Endocrinol 173:371–377. doi: 10.1016/j.ygcen.2011.06.015 CrossRefPubMedGoogle Scholar
  33. Narayan EJ, Cockrem JF, Hero JM (2012) Effects of temperature on urinary corticosterone metabolite responses to short-term capture and handling stress in the cane toad (Rhinella marina). Gen Comp Endocrinol 178:301–305. doi: 10.1016/j.ygcen.2012.06.014 CrossRefPubMedGoogle Scholar
  34. 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. doi: 10.1371/journal.pone.0092090 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Nowakowski AJ, Otero Jiménez B, Allen M, Diaz-Escobar M, Donnelly MA (2013) Landscape resistance to movement of the poison frog, Oophaga pumilio, in the lowlands of northeastern Costa Rica. Anim Conserv 16:188–197. doi: 10.1111/j.1469-1795.2012.00585.x CrossRefGoogle Scholar
  36. Pasukonis A, Loretto MC, Landler L, Ringler M, Hodl W (2014) Homing trajectories and initial orientation in a neotropical territorial frog, Allobates femoralis (Dendrobatidae). Front Zool 11:29. doi: 10.1186/1742-9994-11-29 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pettit LJ, Greenlees MJ, Shine R (2016) The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments? Behav Ecol Sociobiol 71:1–14. doi: 10.1007/s00265-016-2245-5 Google Scholar
  38. 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. doi: 10.1111/j.1442-9993.2007.01664.x CrossRefGoogle Scholar
  39. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803. doi: 10.1038/439803a CrossRefPubMedGoogle Scholar
  40. Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721. doi: 10.1111/j.1461-0248.2005.00774.x CrossRefGoogle Scholar
  41. Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391. doi: 10.1023/B:BINV.0000034618.93140.a5 CrossRefGoogle Scholar
  42. Richards S, Sinsch U, Alford R (1994) Radio tracking. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS (eds) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Books, Washington, DC, pp 155–158Google Scholar
  43. Roland J, Keyghobadi N, Fownes S (2000) Alpine Parnassius butterfly dispersal: effects of landscape and population size. Ecology 81:1642–1653. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  44. Schreiber SJ, Lloyd-Smith JO (2009) Invasion dynamics in spatially heterogeneous environments. Am Nat 174:490–505. doi: 10.1086/605405 CrossRefPubMedGoogle Scholar
  45. Seabrook W (1991) Range expansion of the introduced cane toad Bufo marinus in New South Wales. Aust Zool 27:58–62. doi: 10.7882/AZ.1991.008 CrossRefGoogle Scholar
  46. Seabrook WA, Dettmann EB (1996) Roads as activity corridors for cane toads in Australia. J Wildl Manag 60:363–368. doi: 10.2307/3802236 CrossRefGoogle Scholar
  47. Shine R, Brown GP, Phillips BL (2011) An evolutionary process that assembles phenotypes through space rather than through time. Proc Natl Acad Sci USA 108:5708–5711. doi: 10.1073/pnas.1018989108 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Simberloff D, Maris V, Martin JL (2013) Inaction ≠ caution: response to Larson, Kueffer, and the ZiF Working Group on Ecological Novelty. Trends Ecol Evol 28:257. doi: 10.1016/j.tree.2013.02.006 CrossRefPubMedGoogle Scholar
  49. Smith J, Phillips B (2006) Toxic tucker: the potential impact of cane toads on Australian reptiles. Pac Conserv Biol 12:40–49. doi: 10.1071/PC060040 CrossRefGoogle Scholar
  50. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W. H. Freeman, New YorkGoogle Scholar
  51. Sol D, Bacher S, Reader SM, Lefebvre L (2008) Brain size predicts the success of mammal species introduced into novel environments. Am Nat 172:S63–S71. doi: 10.1086/588304 CrossRefPubMedGoogle Scholar
  52. 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. doi: 10.1073/pnas.0408145102 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tingley R, Phillips BL, Letnic M, Brown GP, Shine R, Baird SJE, Cadotte M (2013) Identifying optimal barriers to halt the invasion of cane toads Rhinella marina in arid Australia. J Appl Ecol 50:129–137. doi: 10.1111/1365-2664.12021 CrossRefGoogle Scholar
  54. 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. doi: 10.1111/j.1466-8238.2010.00530.x Google Scholar
  55. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  56. 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 274:1413–1419. doi: 10.1098/rspb.2007.0114 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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. doi: 10.1086/527494 CrossRefPubMedGoogle Scholar
  58. van Beurden EK, Grigg GC (1980) An isolated and expanding population of the introduced toad Bufo marinus in New South Wales. Wildl Res 7:305–310. doi: 10.1071/WR9800305 CrossRefGoogle Scholar
  59. Vilà M, Basnou C, Pyšek P, Josefsson M, Genovesi P, Gollasch S, Nentwig W, Olenin S, Roques A, Roy D (2009) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144. doi: 10.1890/080083 CrossRefGoogle Scholar
  60. 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. doi: 10.1098/rsbl.2013.1014 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Westphal MI, Browne M, MacKinnon K, Noble I (2007) The link between international trade and the global distribution of invasive alien species. Biol Invasions 10:391–398. doi: 10.1007/s10530-007-9138-5 CrossRefGoogle Scholar
  62. White AW, Shine R (2009) The extra-limital spread of an invasive species via ‘stowaway’ dispersal: toad to nowhere? Anim Conserv 12:38–45. doi: 10.1111/j.1469-1795.2008.00218.x CrossRefGoogle Scholar
  63. Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar
  64. Zenni RD, Nuñez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122:801–815. doi: 10.1111/j.1600-0706.2012.00254.x CrossRefGoogle Scholar
  65. Zollner PA, Lima SL (1999) Search strategies for landscape-level interpatch movements. Ecology 80:1019–1030CrossRefGoogle Scholar
  66. Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resumé of native populations. Smithsonian Contrib Zool 284:1–58Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia

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