Abstract
Invasive species can fundamentally change ecosystems, but there remains surprisingly little understanding of how they alter ecosystems through time. New Zealand mudsnails (NZMS, Potamopyrgus antipodarum) are invading North American aquatic ecosystems with potentially enormous impacts on stream communities and ecosystems. Here we present a unique 10 year time series of stream benthic invertebrates in two sites in a California stream—one invaded site where NZMS populations boomed and then busted, and one upstream reference site that was not invaded to the same degree. As NZMS populations rose and fell, the abundance of native grazing herbivores crashed and then recovered, evidence of direct negative competitive impacts of NZMS. However, NZMS had a positive indirect effect on piercing herbivores, probably mediated by a shift in the dominant algal type. Retrospective stable isotope analyses and Bayesian isotopic mixing models revealed that NZMS invasion decreased the reliance of native taxa, from a variety of functional feeding groups, on periphyton-derived carbon. Furthermore, NZMS invasion was associated with depleted nitrogen stable isotope signatures, evidence that NZMS alter stream ecosystem nitrogen cycling. The reference site did not exhibit these community- or ecosystem-level dynamics. Thus, invasive herbivores can have strong top-down and bottom-up influences on invaded ecosystems, but these impacts can be extremely temporally dynamic.
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References
Arango CP, Tank JL, Riley LA, Hall RO Jr (2009) Herbivory by an invasive snail increases nitrogen fixation in a nitrogen-limited stream. Can J Fish Aquat Sci 66:1309–1317
Bruce RL, Moffit CM, Dennis B (2009) Survival and passage of ingested New Zealand mudsnails through the intestinal tract of rainbow trout. North Am J Aquac 71:287–301
Byrnes JE, Reynolds PL, Stachowicz JJ (2007) Invasions and extinctions reshape coastal marine food webs. PLoS ONE 2:e295
Carlsson NOL, Brönmark C, Hansson L-A (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580
Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey-an acquired taste? Front Ecol Environ 7:525–532
Carlsson NOL, Bustamante H, Strayer DL, Pace ML (2011) Biotic resistance on the increase: native predators structure invasive zebra mussel populations. Freshw Biol 56:1630–1637
Casey MM, Post DM (2011) The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth Sci Rev 106:131–148
Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subarctic islands from grassland to tundra. Science 307:1959–1961
Cross WF, Rosi-Marshall EJ, Behn KE, Kennedy TA, Hall RO Jr, Fuller AE, Baxter CV (2010) Invasion and production of New Zealand mud snails in the Colorado River, Glen Canyon. Biol Invasions 12:3033–3043
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Francis TB, Schindler DE, Holtgrieve GW, Larson ER, Scheuerell MD, Semmens BX, Ward EJ (2011) Habitat structure determines resource use by zooplankton in temperate lakes. Ecol Lett 14:364–372
Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140
Hall RO Jr, Tank JL, Dybdahl MF (2003) Exotic snails dominate nitrogen and carbon cycling in a highly productive stream. Front Ecol Environ 1:407–411
Hall RO Jr, Dybdahl MF, VanderLoop MC (2006) Extremely high secondary production of introduced snails in rivers. Ecol Appl 16:1121–1131
Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843
Herbst DB, Bogan MT, Lusardi RA (2008) Low specific conductivity limits growth and survival of the New Zealand mud snail from the Upper Owens River, California. West North Am Nat 68:324–333
Herbst DB, Silldorff EL, Cooper SD (2009) The influence of introduced trout on the benthic communities of paired headwater streams in the Sierra Nevada of California. Freshw Biol 54:1324–1342
Kerans BL, Dybdahl MF, Gangloff MM, Jannot JE (2005) Potamopyrgus antipodarum: distribution, density, and effects on native macroinvertebrate assemblages in the Greater Yellowstone Ecosystem. J North Am Benthol Soc 24:123–138
McCutchan JH Jr, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390
Merritt RW, Cummins KW, Berg MB (2008) An introduction to the aquatic insects of North America, 4th edn. Kendall Hunt Publishing, Dubuque
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480
Morrison LW (2002) Long-term impacts of an arthropod-community invasion by the imported fire ant, Solenopsis invicta. Ecology 83:2337–2345
Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing. Vienna, Austria
Riley LA, Dybdahl MF, Hall RO Jr (2008) Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails. J North Am Benthol Soc 27:509–520
Schmidt SN, Olden JD, Solomon CT, Vander Zanden MJ (2007) Quantitative approaches to the analysis of stable isotope food web data. Ecology 88:2793–2802
Schrieber ESG, Lake PS, Quinn GP (2002) Facilitation of native stream fauna by an invading species? Experimental investigations of the interaction of the snail, Potamopyrgus antipodarum (Hydrobiidae) with native benthic fauna. Biol Invasions 4:317–325
Semmens BX, Ward EJ, Moore JW, Darimont CT (2009) Quantifying inter- and intra-population niche variability using hierarchical Bayesian stable isotope mixing models. PLoS ONE 4:e6187
Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268
Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—Population crashes of established introduced species. Biol Invasions 6:161–172
Strayer DL (2009) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Front Ecol Evol 7:135–141
Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651
Strayer DL, Cid N, Malcom HM (2011) Long-term changes in a population of an invasive bivalve and its effects. Oecologia 165:1063–1072
R Development Core Team (2010) R: a language and environment for statistical computing, version 2.11.1. R Foundation for Statistical Computing, Vienna
Thorpe JH, Covich AP (2009) Ecology and classification of North American freshwater invertebrates, 2nd edn. Academic Press, San Diego
Twardochleb LA, Novak M, Moore JW (in press) Using the functional response of a consumer to predict biotic resistance to invasive prey. Ecol Appl
Ventura M, Jeppesen E (2009) Effects of fixation on freshwater invertebrate carbon and nitrogen isotope composition and its arithmetic correction. Hydrobiologia 632:297–308
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New Jersey
Acknowledgments
We thank the field crews for helping collecting and sorting the benthic invertebrates. Funding for the long-term invertebrate monitoring was provided by the Lahontan Regional Water Quality Control Board and for the stable isotope analyses by California Sea Grant College Program (R/ANS-131PD). Eric Ward provided critical assistance with quantitative analyses. We appreciate constructive comments from several anonymous reviewers. We thank the University of California at Davis Stable Isotope Facility for running stable isotope samples.
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Moore, J.W., Herbst, D.B., Heady, W.N. et al. Stream community and ecosystem responses to the boom and bust of an invading snail. Biol Invasions 14, 2435–2446 (2012). https://doi.org/10.1007/s10530-012-0240-y
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DOI: https://doi.org/10.1007/s10530-012-0240-y