Biological Invasions

, Volume 17, Issue 1, pp 1–8 | Cite as

Priority effects can lead to underestimation of dispersal and invasion potential

  • Ceridwen I. Fraser
  • Sam C. Banks
  • Jonathan M. Waters
Perpectives and paradigms

Abstract

Molecular analyses are frequently used to assess biological gene flow and dispersal, yet recent data suggest that the operation of density-dependent priority effects often leads to underestimation of species movement patterns and associated invasive potential. Although individual movement is broadly considered to promote connectivity among populations, emerging genetic evidence on a range of scales indicates that it often fails to do so; instead, it can be a strategy that allows first colonizers to wedge a ‘foot in the door’ when new space becomes available. Founding lineages can then rapidly dominate, blocking colonization by later arrivals; subsequent invasion opportunities may be contingent on the extirpation of locals. Many contemporary studies, however, ignore the role of such density-dependent priority effects, and thus fail to assess major differences between movement and establishment. Understanding the role of these processes in the successful establishment of dispersing organisms is critical if we are to predict distributional range shifts and deal with invasive pest species.

Keywords

Priority effect Colonization Disturbance Invasion Reinvasion Establishment 

References

  1. Abdelkrim J, Pascal M, Samadi S (2007) Establishing causes of eradication failure based on genetics: case study of ship rat eradication in Ste. Anne Archipelago. Conserv Biol 21:719–730PubMedCrossRefGoogle Scholar
  2. Almany GR (2003) Priority effects in coral reef fish communities. Ecology 84:1920–1935CrossRefGoogle Scholar
  3. Almany GR, Berumen ML, Thorrold SR et al (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744PubMedCrossRefGoogle Scholar
  4. Amstrup S, MacDonald L, Manly B (2005) Handbook of Capture-Recapture Analysis. Princeton University Press, New JerseyGoogle Scholar
  5. Banks SC, Lindenmayer DB (2013) Inbreeding avoidance, patch isolation and matrix permeability influence dispersal and settlement choices by male agile antechinus in a fragmented landscape. J Anim Ecol 83:515–524CrossRefGoogle Scholar
  6. Barber PH, Palumbi SR, Erdmann MV et al (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674PubMedCrossRefGoogle Scholar
  7. Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561PubMedCrossRefGoogle Scholar
  8. Boessenkool S, Austin JJ, Worthy TH et al (2009a) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proc R Soc Biol Sci Ser B 276:815–821CrossRefGoogle Scholar
  9. Boessenkool S, Star B, Waters JM et al (2009b) Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes). Mol Ecol 18:2390–2400PubMedCrossRefGoogle Scholar
  10. Booth JD, Ovenden JR (2000) Distribution of Jasus spp. (Decapoda : Palinuridae) phyllosomas in southern waters: implications for larval recruitment. Mar Ecol Prog Ser 200:241–255CrossRefGoogle Scholar
  11. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225PubMedCrossRefGoogle Scholar
  12. Buckley HL, Paterson AM, Cruickshank RH et al (2013) The founder space race: a response to Waters et al. Trends Ecol Evol 28:189–190PubMedCrossRefGoogle Scholar
  13. Buonaccorsi VP, Kimbrell CA, Lynn EA et al (2005) Limited realized dispersal and introgressive hybridization influence genetic structure and conservation strategies for brown rockfish, Sebastes auriculatus. Conserv Genet 6:697–713CrossRefGoogle Scholar
  14. Burgman MA, McCarthy MA, Robinson A et al (2013) Improving decisions for invasive species management: reformulation and extensions of the Panetta-Lawes eradication graph. Divers Distrib 19:603–607CrossRefGoogle Scholar
  15. Calmet C, Pascal M, Samadi S (2001) Is it worth eradicating the invasive pest Rattus norvegicus from Molène archipelago? Genetic structure as a decision-making tool. Biodivers Conserv 10:911–928CrossRefGoogle Scholar
  16. Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498PubMedCrossRefGoogle Scholar
  17. Clobert J, Le Galliard J-F, Cote J et al (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209PubMedCrossRefGoogle Scholar
  18. De Meester L, Gomez A, Okamura B et al (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol Int J Ecol 23:121–135CrossRefGoogle Scholar
  19. Donlan CJ, Tershy BR, Campbell K et al (2003) Research for requiems: the need for more collaborative action in eradication of invasive species. Conserv Biol 17:1850–1851CrossRefGoogle Scholar
  20. Eitam A, Blaustein L, Mangel M (2005) Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146:36–42PubMedCrossRefGoogle Scholar
  21. Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630PubMedCrossRefGoogle Scholar
  22. Esher RJ, Wolfe JL, Layne JN (1978) Swimming behavior of rice rats (Oryzomys palustris) and cotton rats (Sigmodon hispidus). J Mammal 59:551–558CrossRefGoogle Scholar
  23. Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351PubMedCrossRefGoogle Scholar
  24. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  25. Fraser CI, Nikula R, Spencer HG et al (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc Natl Acad Sci USA 106:3249–3253PubMedCentralPubMedCrossRefGoogle Scholar
  26. Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc Biol Sci Ser B 278:649–655CrossRefGoogle Scholar
  27. Fretwell SD, Calver JS (1969) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:37–44CrossRefGoogle Scholar
  28. Gauffre B, Petit E, Brodier S et al (2009) Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proc R Soc B-Biol Sci 276:3487–3494CrossRefGoogle Scholar
  29. Geange SW, Stier AC (2009) Order of arrival affects competition in two reef fishes. Ecology 90:2868–2878PubMedCrossRefGoogle Scholar
  30. Glen AS, Atkinson R, Campbell KJ et al (2013) Eradicating multiple invasive species on inhabited islands: the next big step in island restoration? Biol Invasions 15:2589–2603Google Scholar
  31. Hallatschek O, Hersen P, Ramanathan S et al (2007) Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci USA 104:19926–19930PubMedCentralPubMedCrossRefGoogle Scholar
  32. Hardouin EA, Chapuis JL, Stevens MI et al (2010) House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion. BMC Evol Biol 10:325PubMedCentralPubMedCrossRefGoogle Scholar
  33. Harris DB, Gregory SD, Bull LS et al (2012) Island prioritization for invasive rodent eradications with an emphasis on reinvasion risk. Biol Invasions 14:1251–1263CrossRefGoogle Scholar
  34. Hewitt GM (1993) Postglacial distribution and species substructure: lessons from pollen, insects and hybrid zones. In: Lees DR, Edwards D (eds) Evolutionary Patterns and Processes. Academic Press, London, pp 97–103Google Scholar
  35. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  36. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  37. Howald G, Donlan CJ, Galvan JP et al (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268PubMedCrossRefGoogle Scholar
  38. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  39. Keitt B, Campbell K, Saunders A et al (2011) The Global Islands Invasive Vertebrate Eradication Database: a tool to improve and facilitate restoration of island ecosystems. In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 74–77Google Scholar
  40. Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein’s bat (Myotis bechsteinii). Mol Ecol 14:3943–3950PubMedCrossRefGoogle Scholar
  41. Kueffer C (2013) Integrating natural and social sciences for understanding and managing plant invasions. In: Larrue S (ed) Biodiversity and Society in the Pacific Islands. ANU ePress, Canberra, pp 71–95Google Scholar
  42. Kuussaari M, Nieminen M, Hanski I (1996) An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J Anim Ecol 65:791–801CrossRefGoogle Scholar
  43. Lee WG, Tanentzap AJ, Heenan PB (2012) Plant radiation history affects community assembly: evidence from the New Zealand alpine. Biol Lett 8:558–561PubMedCentralPubMedCrossRefGoogle Scholar
  44. Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051PubMedCrossRefGoogle Scholar
  45. Miller MP, Haig SM, Ledig DB et al (2011) Will an “island” population of voles be recolonized if eradicated? insights from molecular genetic analyses. J Wildl Manag 75:1812–1818CrossRefGoogle Scholar
  46. Münkemüller T, Travis JMJ, Burton OJ et al (2011) Density-regulated population dynamics and conditional dispersal alter the fate of mutations occurring at the front of an expanding population. Heredity 106:678–689PubMedCentralPubMedCrossRefGoogle Scholar
  47. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  48. Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proc R Soc Biol Sci Ser B 279:749–758CrossRefGoogle Scholar
  49. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697PubMedCentralPubMedCrossRefGoogle Scholar
  50. Pulliam HR, Danielson BJ (1991) Sources, sinks, and habitat selection - a landscape perspective on population dynamics. Am Nat 137:S50–S66CrossRefGoogle Scholar
  51. Ricklefs RE (2010) Dynamics of colonization and extinction on islands: insights from Lesser Antillean birds. In: Losos JB, Ricklefs RE (eds) The Theory of Island Biogeography Revisited. Princeton University Press, Princeton, pp 388–414Google Scholar
  52. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242PubMedCrossRefGoogle Scholar
  53. Roques L, Garnier J, Hamel F et al (2012) Allee effect promotes diversity in traveling waves of colonization. Proc Natl Acad Sci USA 109:8828–8833PubMedCentralPubMedCrossRefGoogle Scholar
  54. Russell JC, Towns DR, Clout MN (2008) Review of rat invasion biology: implications for island biosecurity. Science for Conservation, 286. Department of Conservation, WellingtonGoogle Scholar
  55. Russell JC, Miller SD, Harper GA et al (2010) Survivors or reinvaders? Using genetic assignment to identify invasive pests following eradication. Biol Invasions 12:1747–1757CrossRefGoogle Scholar
  56. Shulman MJ, Ogden JC, Ebersole JP et al (1983) Priority effects in the recruitment of juvenile coral-reef fishes. Ecology 64:1508–1513CrossRefGoogle Scholar
  57. Tan JQ, Pu ZC, Ryberg WA et al (2012) Species phylogenetic relatedness, priority effects, and ecosystem functioning. Ecology 93:1164–1172PubMedCrossRefGoogle Scholar
  58. Towns DR (2011) Eradications of vertebrate pests from islands around New Zealand: what have we delivered and what have we learned? In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 364–371Google Scholar
  59. Travis JMJ, Munkemuller T, Burton OJ (2010) Mutation surfing and the evolution of dispersal during range expansions. J Evol Biol 23:2656–2667PubMedCrossRefGoogle Scholar
  60. Veale AJ, Clout MN, Gleeson DM (2012) Genetic population assignment reveals a long-distance incursion to an island by a stoat (Mustela erminea). Biol Invasions 14:735–742CrossRefGoogle Scholar
  61. Votier SC, Grecian WJ, Patrick S et al (2011) Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis. Mar Biol 158:355–362CrossRefGoogle Scholar
  62. Waters JM, Fraser CI, Banks SC et al (2013a) The founder space race: a reply to Buckley et al. Trends Ecol Evol 28:190–191PubMedCrossRefGoogle Scholar
  63. Waters JM, Fraser CI, Hewitt GM (2013b) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28:78–85PubMedCrossRefGoogle Scholar
  64. White TA, Perkins SE, Heckel G et al (2013) Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Mol Ecol 22:2971–2985PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Ceridwen I. Fraser
    • 1
  • Sam C. Banks
    • 1
  • Jonathan M. Waters
    • 2
  1. 1.Fenner School of Environment and SocietyAustralian National UniversityCanberraAustralia
  2. 2.Allan Wilson Centre for Molecular Ecology and Evolution, Department of ZoologyUniversity of OtagoDunedinNew Zealand

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