Abstract
The enemy release hypothesis states that invasive species are successful in their new environment because native species are not adapted to utilize the invasive. If true for predators, native predators should have lower feeding rates on the invasive species than a predator from the native range of the invasive species. We tested this hypothesis for zebra mussel (Dreissena polymorpha) by comparing handling time and predation rate on zebra mussels in the laboratory by two North American species (pumpkinseed, Lepomis gibbosus, and rusty crayfish, Orconectes rusticus) and one predator with a long evolutionary history with zebra mussels (round goby, Neogobius melanostomus). Handling time per mussel (7 mm shell length) ranged from 25 to >70 s for the three predator species. Feeding rates on attached zebra mussels were higher for round goby than the two native predators. Medium and large gobies consumed 50–67 zebra mussels attached to stones in 24 h, whereas pumpkinseed and rusty crayfish consumed <11. This supports the hypothesis that the rapid spread of zebra mussels in North America was facilitated by low predation rates from the existing native predators. At these predation rates and realistic goby abundance estimates, round goby could affect zebra mussel abundance in some lakes.
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References
Andraso, G. M., 2005. Summer food habits of pumpkinseeds (Lepomis gibbosus) and bluegills (Lepomis macrochirus) in Presque Isle Bay, Lake Erie. Journal of Great Lakes Research 31: 397–404.
Andraso, G. M., M. T. Ganger & J. Adamczyk, 2011a. Size-selective predation by round gobies (Neogobius melanostomus) on dreissenid mussels in the field. Journal of Great Lakes Research 37: 298–304.
Andraso, G. M., J. Cowles, R. Colt, J. Patel & M. Campbell, 2011b. Ontogenetic changes in pharyngeal morphology correlate with a diet shift. Journal of Great Lakes Research 37: 738–743.
Bartsch, M. R., L. A. Barstch & S. Gutreuter, 2005. Strong effects of predation by fishes on an invasive macroinvertebrate in a large floodplain river. Journal of the North American Benthological Society 24: 168–177.
Blossey, B. & R. Notzold, 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology 83: 887–889.
Boles, L. C. & R. N. Lipcius, 1997. Potential for population regulation of the zebra mussel by finfish and the blue crab in North American estuaries. Journal of Shellfish Research 16: 179–186.
Bunnell, D. B., T. B. Johnson & C. T. Knight, 2005. The impact of introduced round gobies (Neogobius melanostomus) on phosphorus cycling in central Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 62: 15–29.
Carlsson, N. O. L. & D. L. Strayer, 2009. Intraspecific variation in the consumption of exotic prey – a mechanism that increases biotic resistance against invasive species? Freshwater Biology 54: 2315–2319.
Carlsson, N. O. L., H. Bustamante, D. L. Strayer & M. L. Pace, 2011. Biotic resistance on the increase: native predators structure invasive zebra mussel populations. Freshwater Biology 56: 1630–1637.
Colautti, R. I., A. Ricciardi, I. A. Grigorovich & H. J. MacIsaac, 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters 7: 721–733.
Colautti, R. I., I. A. Grigorovich & H. J. MacIsaac, 2006. Propagule pressure: a null model for biological invasions. Biological Invasions 8: 1023–1037.
Connelly, N. A., C. R. O’Neill, B. A. Knuth & T. L. Brown, 2007. Economic impacts of zebra mussels on drinking water treatment and electric power generation facilities. Environmental Management 40: 105–112.
Covich, A. P., L. L. Dye & J. S. Mattice, 1981. Crayfish predation on Corbicula under laboratory conditions. American Midland Naturalist 105: 181–188.
Cox, G. W., 2004. Alien Species and Evolution. Island Press, Washington, DC.
deRivera, C. E., G. M. Ruiz, A. H. Hines & P. Jivoff, 2005. Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86: 3364–3376.
Eggleton, M. A., L. E. Miranda & J. P. Kirk, 2004. Assessing the potential for fish predation to impact zebra mussels (Dreissena polymorpha): insight from bioenergetics models. Ecology of Freshwater Fish 13: 85–95.
French III, J. R. P., 1993. How well can fishes prey on zebra mussels in eastern North America? Fisheries 18: 13–19.
Ghedotti, M. J., J. C. Smihula & G. R. Smith, 1995. Zebra mussel predation by round gobies in the laboratory. Journal of Great Lakes Research 21: 665–669.
Havel, J. E., J. B. Shurin & J. R. Jones, 2005. Environmental limits to a rapidly spreading exotic cladoceran. Ecoscience 12: 376–385.
Hoyle, J. A., J. N. Bowlby & B. J. Morrison, 2008. Lake whitefish and walleye population responses to dreissenid mussel invasion in eastern Lake Ontario. Aquatic Ecosystem Health and Management 11: 403–411.
Idrisi, N., E. L. Mills, L. G. Rudstam & D. J. Stewart, 2001. Impact of zebra mussels (Dreissena polymorpha) on the pelagic trophic levels of Oneida Lake, New York. Canadian Journal of Fisheries and Aquatic Science 58: 1430–1441.
Johnson, T. B., D. B. Bunnell & C. T. Knight, 2005. A potential new energy pathway in central Lake Erie: the round goby connection. Journal of Great Lakes Research 31: 238–251.
Jude, D. J., J. Janssen & G. Crawford, 1995. Ecology, distribution and impact of the newly introduced round and tubenose gobies on the biota of the St. Clair and Detroit rivers. In Munawar, M., T. Edsall & J. Leach (eds), The Lake Huron Ecosystem: Ecology, Fisheries and Management. Ecovision World Monograph Series. SPB Academic Publishing, The Hague: 447–460.
Kennedy, T. A., S. Naeem, K. M. Howe, J. M. H. Knops, D. Tilman & P. Relch, 2002. Biodiversity as a barrier to ecological invasion. Nature 417: 636–638.
Kornis, M. S., N. Mercado-Silva & M. J. Vander Zanden, 2012. Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. Journal of Fish Biology 80: 235–285.
Leach, J. H., 1995. Non-indigenous species in the Great Lakes: were colonization and damage to ecosystem health predictable? Journal of Aquatic Ecosystem Health 4: 117–128.
Lodge, D. M., M. W. Kershner, J. E. Aloi & A. P. Covich, 1994. Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75: 1265–1281.
Love, J. & J. F. Savino, 1993. Crayfish (Orconectes virilis) predation on zebra mussels (Dreissena polymorpha). Journal of Freshwater Ecology 8: 253–259.
MacIsaac, H. J., 1994. Size-selective predation on zebra mussels (Dreissena polymorpha) by crayfish (Orconectes propinquus). Journal of the North American Benthological Society 13: 206–216.
MacIsaac, H. J., 1996. Potential abiotic and biotic impacts of zebra mussels on the inland waters of North America. American Zoologist 36: 287–299.
Magoulick, D. D. & L. C. Lewis, 2002. Predation on exotic zebra mussels by native fishes: effects on predator and prey. Freshwater Biology 47: 1908–1918.
Martin, G. W. & L. D. Corkum, 1994. Predation of zebra mussels by crayfish. Canadian Journal of Zoology 72: 1867–1871.
Mills, E. L., J. L. Forney & K. T. Holeck, 2013. Oneida Lake: a century of biotic introductions and ecosystem change. In Rudstam, L. G., E. L. Mills, J. R. Jackson & D. J. Stewart (eds), Oneida Lake: Long-Term Dynamics of a Managed Ecosystem and Its Fisheries. American Fisheries Society, Bethesda (in press).
Naddafi, R. & L. G. Rudstam, 2013. Predator diversity effects in an exotic freshwater food web. PLoS ONE: e72599. doi:10.1371/journal.pone.0072599.
Naddafi, R., P. Eklöv & K. Pettersson, 2007. Non-lethal predator effects on the feeding rate and prey selection of the exotic zebra mussel Dreissena polymorpha. Oikos 116: 1289–1298.
Naddafi, R., K. Pettersson & P. Eklöv, 2010. Predation and physical environment structure the density and population size structure of zebra mussels. Journal of the North American Benthological Society 29: 444–453.
Naddafi, R., T. Blenckner, P. Eklöv & K. Pettersson, 2011. Physicochemical properties determine zebra mussel invasion success in lakes. Hydrobiologia 669: 227–236.
Naddafi, R., W. Goedkoop, U. Grandin & P. Eklöv, 2012. Variation in tissue stoichiometry and condition of zebra mussels in invaded Swedish lakes. Biological Invasions 14: 2117–2131.
Nagelkerke, L. A. J. & F. A. Sibbing, 1996. Efficiency of feeding on zebra mussel (Dreissena polymorpha) by common bream (Abramis brama), white bream (Blicca bjoerkna), and roach (Rutilus rutilus): the effects of morphology and behavior. Canadian Journal of Fisheries and Aquatic Sciences 53: 2847–2861.
Nyström, P., 2002. Ecology. In Holdich, D. M. (ed.), Biology of Freshwater Crayfish. Blackwell Science, Oxford: 192–224.
Perry, W. L., D. M. Lodge & G. A. Lamberti, 1997. Impact of crayfish predation on exotic zebra mussels and native invertebrates in a lake-outlet stream. Canadian Journal of Fisheries and Aquatic Sciences 54: 120–125.
Peterson, A. T. & D. A. Vieglais, 2001. Predicting species invasions using ecological niche modeling. BioScience 51: 363–371.
Piesik, Z., 1974. The role of the crayfish Orconectes limosus (Raf.) in extinction of Dreissena polymorpha (Pall.) subsisting on steelon-net. Polskie Archiwum Hydrobiologii 21: 401–410.
Pothoven, S. A. & C. P. Madenjian, 2008. Changes in consumption by alewives and lake whitefish after dreissenid mussel invasions in Lakes Michigan and Huron. North American Journal of Fisheries Management 28: 308–320.
Ray, W. J. & L. D. Corkum, 1997. Predation of zebra mussels by round gobies, Neogobius melanostomus. Environmental Biology of Fishes 50: 267–273.
Reynolds, J. D. & R. Donohoe, 2001. Crayfish predation experiments on the introduced zebra mussel, Dreissena polymorpha, in Ireland, and their potential for biocontrol. Bulletin Francais de la Pêche et de la Pisciculture 361: 669–681.
Rudstam, L. G., 2013. Limnological data and depth profile from Oneida Lake, New York, 1975–2011. Knowledge Network for Biocomplexity. http://knb.ecoinformatics.org/knb/metacat/kgordon.35.42/default.
Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, D. E. McCauley, P. O’Neil, I. M. Parker, J. N. Thompson & S. G. Weller, 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332.
Schreiber, S., T. Odelstrom, K. Pettersson & D. Eichelberg, 1998. The zebra mussel Dreissena polymorpha as a food source for the signal crayfish Pacifastacus leniusculus in Lake Erken – laboratory experiments. Ergebnisse der Limnologie 51: 169–176.
Simberloff, D. & L. Gibbons, 2004. Now you see them, now you don’t – population crashes of established introduced species. Biological Invasions 6: 161–172.
Strayer, D. L., N. Cid & H. M. Malcom, 2011. Long-term changes in a population of an invasive bivalve and its effects. Oecologia 165: 1063–1072.
Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, E. L. Mills, K. T. Holeck, J. R. Liebig, I. A. Grigorovich & H. Ojaveer, 2002. Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Science 59: 1209–1228.
Walsh, M. G., D. E. Dittman & R. O. O’Gorman, 2007. Occurrence and food habits of the round goby in the profundal zone of southwestern Lake Ontario. Journal of Great Lakes Research 33: 83–92.
Watzin, M. C., K. Joppe-Mercure, J. Rowder, B. Lancaster & L. Bronson, 2008. Significant fish predation on zebra mussels Dreissena polymorpha in Lake Champlain, U.S.A. Journal of Fish Biology 73: 1585–1599.
Zipser, E. & G. J. Vermeij, 1978. Crushing behaviour of tropical and temperate crabs. Journal of Experimental Marine Biology and Ecology 31: 155–172.
zu Ermgassen, P. S. E. & D. C. Aldridge, 2011. Predation by the invasive American signal crayfish, Pacifastacus leniusculus Dana, on the invasive zebra mussel, Dreissena polymorpha Pallas: the potential for control and facilitation. Hydrobiologia 658: 303–315.
Acknowledgments
We thank Thomas Brooking, Scott Krueger, James Watkins, William Fetzer, Nazila Koupayeh, and Dana Seidel for assistance in the field and Brian Young and Bill Thelen for help with the experimental setup. We are also grateful to the two anonymous reviewers as well as Matthew Kornis and the editor John Havel for valuable comments, which helped improve the manuscript. We thank Kjell Leonardsson for helpful discussions. This research was supported by the Swedish Research Council (VR) (registration number: 623-2008-486) to RN and a grant from the Cornell University Agricultural Experiment Station to LGR.
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Naddafi, R., Rudstam, L.G. Predation on invasive zebra mussel, Dreissena polymorpha, by pumpkinseed sunfish, rusty crayfish, and round goby. Hydrobiologia 721, 107–115 (2014). https://doi.org/10.1007/s10750-013-1653-z
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DOI: https://doi.org/10.1007/s10750-013-1653-z