Skip to main content

Advertisement

SpringerLink
Log in

Comparing residence time and natural enemies between low- and high- density invasions

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Ecological and historical factors influence the probability that a known invader will experience success in new locations. Using field and laboratory studies, we investigated how residence time and natural enemies (co-evolved castrating parasite, and native crabs) differ between two introduced populations of the intertidal snail, Batillaria attramentaria. The populations have substantially different invasion histories (~ 10 vs. > 80 years) and exhibit markedly different densities and tidal distributions. The less-dense, vertically-restricted population was recently introduced, and thus has potentially had less opportunity to fill the fundamental niche at that site. However, no increase in density or intertidal range occurred in this population over 10 years, suggesting that it had reached its realized niche. The newer population experienced much greater effects of native cancrid crabs than the older, high-density population, particularly below the minimum tidal elevation of observed snail distribution, where crabs were found in the greatest densities. Prevalence of parasite infection did not differ between populations. This is the first study documenting effects of predators on this invasive snail, which is widespread along coastlines of the northeast Pacific, whereas previous studies have suggested that the primary restriction on population growth rate was likely to be parasitic castration. Further, this study supports the general understanding that, while novel predators can reduce the impacts or population growth rates of invasive species, such top-down effects are not likely to preclude persistence at a given site.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  Google Scholar 

  • Bulthuis DA (2013) The ecology of Padilla Bay, Washington: an estuarine profile of a National Estuarine Research Reserve. Washington State Department of Ecology, Padilla Bay National Estuarine Research Reserve, Mt. Vernon, Washington

  • Byers JE (1999) The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial species. Biol Invasions 1:339–352

    Article  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156

    Article  Google Scholar 

  • Byers JE, Goldwasser L (2001) Exposing the mechanism and timing of impact of nonindigenous species on native species. Ecology 82:1330–1343

    Article  Google Scholar 

  • Byers JE, Malek AJ, Quevillon LE et al (2015a) Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos 124:1511–1519

    Article  Google Scholar 

  • Byers JE, Smith RS, Pringle JM et al (2015b) Invasion expansion: time since introduction best predicts global ranges of marine invaders. Sci Rep 5:12346

    Article  Google Scholar 

  • Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037

    Article  Google Scholar 

  • Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710–723

    Article  Google Scholar 

  • Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192

    Article  Google Scholar 

  • Dinnel PA (2000) Padilla Bay Molluscs: a review, with emphasis on the bivalves. Padilla Bay National Estuarine Research Reserve, Mount Vernon

    Google Scholar 

  • Dinnel PA, McMillan RO, Armstrong DA et al (1986) Padilla Bay Dungeness crab, Cancer magister, habitat study. Padilla Bay National Estuarine Research Reserve, Mount Vernon

    Google Scholar 

  • Fabian RA (2016) Ecological effects of an invasive mud snail and its body-snatching parasites: implications for organic matter cycling in a eutrophic estuary. Doctoral Dissertation, University of California, Santa Cruz

  • Hechinger RF (2007) Annotated key to the trematode species infecting Batillaria attramentaria (Prosobranchia: Batillariidae) as first intermediate host. Parasitol Int 56:287–296

    Article  Google Scholar 

  • Holsman KK, Armstrong DA, Beauchamp DA, Ruesink JL (2003) The necessity for intertidal foraging by estuarine populations of subadult Dungeness crab, Cancer magister: evidence from a bioenergetics model. Estuaries 26:1155–1173

    Article  Google Scholar 

  • Holsman KK, McDonald PS, Armstrong DA (2006) Intertidal migration and habitat use by subadult Dungeness crab Cancer magister in a NE Pacific estuary. Mar Ecol Prog Ser 308:183–195

    Article  Google Scholar 

  • Hunt CE, Yamada SB (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biol Invasions 5:33–43

    Article  Google Scholar 

  • Jensen GC, McDonald PS, Armstrong DA (2007) Biotic resistance to green crab, Carcinus maenas, in California bays. Mar Biol 151:2231–2243

    Article  Google Scholar 

  • Kimbro DL, Cheng BS, Grosholz ED (2013) Biotic resistance in marine environments. Ecol Lett 16:821–833

    Article  Google Scholar 

  • Kincaid T (1968) The ecology of Willapa Bay, Washington, in relation to the oyster industry. [s.n], Seattle, Washington

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • Lin PP (2006) Prevalence of parasitic larval trematodes in Batillaria attramentaria throughout Elkhorn Slough. Elkhorn Slough National Estuarine Research Reserve, Mount Vernon

    Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  Google Scholar 

  • Miura O, Kuris AM, Torchin ME et al (2006) Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc Biol Sci 273:1323–1328

    Article  Google Scholar 

  • McPeek KC, McDonald PS, Vanblaricom GR (2015) Aquaculture disturbance impacts the diet but not ecological linkages of a ubiquitous predatory fish. Estuar Coasts 38(5):1520–1534

    Article  Google Scholar 

  • Moyle PB, Light T (1996) Fish invasions in California: Do abiotic factors determine success? Ecology 77:1666–1670

    Article  Google Scholar 

  • ONRC Olympic Natural Resources Center (2008) Willapa Bay 30 foot (9.14 meter) Intertidal bathymetry — localized MLLW. Raster digital data. https://www.onrc.washington.edu/clearinghouse/pub/onrc/WillapaBayGIS/wb_mllw_0207.zip

  • PBNERR (2008) Padilla Bay National Marine Estuarine Research Reserve Management Plan. Padilla Bay NERR, Mt. Vernon

    Google Scholar 

  • Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433

    Article  Google Scholar 

  • Pyšek P, Jarošik V (2005) Residence time determines the distribution of alien plants. In: Invasive plants: ecological and agricultural aspects. Birkhauser Verlag, Basel, pp 77–96

  • Rooper CN, Armstrong DA, Gunderson DR (2002) Habitat use by juvenile Dungeness crabs in coastal nursery estuaries. In: Crabs in Cold water regions: biology, management, and economics. Alaska Sea Grant College Program, University of Alaska Fairbanks, pp 609–629

  • Ruesink JL, Hong J-S, Wisehart L et al (2010) Congener comparison of native (Zostera marina) and introduced (Z. japonica) eelgrass at multiple scales within a Pacific Northwest estuary. Biol Invasions 12:1773–1789

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  • Suwa T, Louda SM (2012) Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 169:467–476

    Article  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  Google Scholar 

  • Thuiller W, Richardson DM, Pyšek P et al (2005) Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Glob Change Biol 11:2234–2250

    Article  Google Scholar 

  • Torchin ME, Byers JE, Huspeni TC (2005) Differential parasitism of native and introduced snails: replacement of a parasite fauna. Biol Invasions 7:885–894

    Article  Google Scholar 

  • White J, Ruesink JL, Trimble AC (2009) The nearly forgotten oyster: Ostrea lurida Carpenter 1864 (Olympia Oyster) history and management in Washington State. J Shellfish Res 28(1):43–49

    Article  Google Scholar 

  • Whittaker RH (1967) Gradient analysis of vegetation. Biol Rev 49:207–264

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wilson JRU, Richardson DM, Rouget M et al (2007) Residence time and potential range: crucial considerations in modelling plant invasions. Divers Distrib 13:11–22

    Article  Google Scholar 

  • Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7:369–392

    Article  Google Scholar 

  • Wonham MJ, O’Connor M, Harley CDG (2005) Positive effects of a dominant invader on introduced and native mudflat species. Mar Ecol Prog Ser 289:109–116

    Article  Google Scholar 

  • Yamada SB, Sankurathri CS (1977) Direct development in the intertidal gastropod Batillaria zonalis (Bruguiere, 1792). Veliger 20:179

    Google Scholar 

  • Yamada S, Boulding E (1998) Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs. J Exp Mar Biol Ecol 220:191–211

    Article  Google Scholar 

  • Zenni RD, Nuñez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122:801–815

    Article  Google Scholar 

Download references

Acknowledgements

The authors are very grateful for assistance provided by M. Hannam and S. Shull (GIS), J. Heckes (site access), R. Theobald (analysis), R. Davis, D. Grason, and M. Flora-Tostado (field assistance). We appreciate the efforts by E. Carrington, J. Olden, M. Hannam, K. Wasson, and two anonymous reviewers, who provided helpful suggestions for improvement of the manuscript. Students at Shannon Point Marine Center, and the University of Washington, assisted with field and laboratory data collection, particularly A. Gehman, and we thank them for their contributions. A portion of this research was conducted in the National Estuarine Research Reserve System under an award from the Estuarine Reserves Division, Office of Ocean and Coastal Resource Management, National Ocean Service, National Oceanic and Atmospheric Administration.

Author information

Authors and Affiliations

  1. Washington Sea Grant, University of Washington, 3716 Brooklyn Avenue N.E, Seattle, WA, 98105-6716, USA

    Emily W. Grason

  2. Program on the Environment, University of Washington, Box 355679, Seattle, WA, 98195-5679, USA

    P. Sean McDonald

  3. Department of Biology, University of Washington, Box 351800, 24 Kincaid Hall, Seattle, WA, 98195-1800, USA

    Jennifer L. Ruesink

Authors
  1. Emily W. Grason
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Sean McDonald
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer L. Ruesink
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emily W. Grason.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grason, E.W., McDonald, P. & Ruesink, J.L. Comparing residence time and natural enemies between low- and high- density invasions. Biol Invasions 20, 3315–3330 (2018). https://doi.org/10.1007/s10530-018-1776-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1776-2

Keywords

Search

Navigation