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Experimental evaluation of the effects of the novel predators, round goby and mud crab on benthic invertebrates in the Gulf of Riga, Baltic Sea

Published online by Cambridge University Press:  22 December 2017

Kristiina Nurkse*
Affiliation:
Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia
Jonne Kotta
Affiliation:
Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia
Merli Rätsep
Affiliation:
Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia
Ilmar Kotta
Affiliation:
Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia
Randel Kreitsberg
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51020 Tartu, Estonia Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Rannu, 61117 Tartu, Estonia
*
Correspondence should be addressed to: K. Nurkse, Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia email: [email protected]

Abstract

The number of non-indigenous aquatic species (NIS) has rapidly increased globally. The majority of published evidence on the effects of NIS on local communities is from single species studies in which the interactive effects of NIS are not considered. Here we present experimental evidence of separate and interactive effects of two widespread non-indigenous benthic predators, the round goby (Neogobius melanostomus) and the North American mud crab (Rhithropanopeus harrisii) on benthic invertebrate communities in a shallow coastal ecosystem of the Gulf of Riga, the Baltic Sea. The two species have recently colonized multiple sub-basins of the Baltic Sea and due to their rapid range expansion, increasing densities and local functional novelty, they are expected to have strong separate or interactive effects on native communities. Our laboratory experiment demonstrated that round goby and mud crab exerted a significant predation pressure on different benthic invertebrate species and the effects of the studied predators were largely independent. Predation was stronger at higher temperature compared with low temperature treatment. Among the studied invertebrate species gammarid amphipods were consumed the most. Interestingly, round goby did not prey on the mud crabs despite a large size difference of the studied predators.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Anderson, M.J. (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Auckland: Department of Statistics, University of Auckland.Google Scholar
Anderson, M.J. and Ter Braak, C. (2003) Permutation tests for multi-factorial analysis of variance. Journal of Statistical Computation and Simulation 73, 85113.Google Scholar
Burlakova, L.E., Tulumello, B.L., Karatayev, A.Y., Krebs, R.A., Schloesser, D.W., Paterson, W.L., Griffith, T.A., Scott, M.W., Crail, T. and Zanatta, D.T. (2014) Competitive replacement of invasive congeners may relax impact on native species: interactions among zebra, quagga, and native unionid mussels. PLoS ONE 9, 120.Google Scholar
Carr, M.H., Neigel, J.E., Estes, J.A., Andelman, S., Warner, R.R. and Largier, J.L. (2003) Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecological Applications 13, 90107.Google Scholar
Clarke, K. and Warwick, R. (2001) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: PRIMER-E.Google Scholar
Collin, S.B. and Johnson, L.E. (2014) Invasive species contribute to biotic resistance: negative effect of caprellid amphipods on an invasive tunicate. Biological Invasions 16, 22092219.Google Scholar
Diggins, T.P., Kaur, J., Chakraborti, R.K. and DePinto, J.V. (2002) Diet choice by the exotic round goby (Neogobius melanostomus) as influenced by prey motility and environmental complexity. Journal of Great Lakes Research 28, 411420.Google Scholar
Doherty, T.S., Glen, A.S., Nimmo, D.G., Ritchie, E.G. and Dickman, C.R. (2016) Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences USA 113, 1126111265.Google Scholar
Foley, C.J., Henebry, M.L., Happel, A., Bootsma, H.A., Czesny, S.J., Janssen, J., Jude, D.J., Rinchard, J. and Höök, T.O. (2017) Patterns of integration of invasive round goby (Neogobius melanostomus) into a nearshore freshwater food web. Food Webs 10, 2638.Google Scholar
Forsström, T., Ahmad, F. and Vasemägi, A. (2017) Invasion genomics: genotyping-by-sequencing approach reveals regional genetic structure and signatures of temporal selection in an introduced mud crab. Marine Biology 164, 186.Google Scholar
Forsström, T., Fowler, A.E., Manninen, I. and Vesakoski, O. (2015) An introduced species meets the local fauna: predatory behavior of the crab Rhithropanopeus harrisii in the Northern Baltic Sea. Biological Invasions 17, 27292741.CrossRefGoogle Scholar
Galil, B.S., Marchini, A., Occhipinti-Ambrogi, A., Minchin, D., Narščius, A., Ojaveer, H. and Olenin, S. (2014) International arrivals: widespread bioinvasions in European Seas. Ethology, Ecology and Evolution 26, 152171.CrossRefGoogle ScholarPubMed
Griffen, B.D. and Byers, J.E. (2009) Community impacts of two invasive crabs: the interactive roles of density, prey recruitment, and indirect effects. Biological Invasions 11, 927940.Google Scholar
Griffen, B.D. and Williamson, T. (2008) Influence of predator density on non-independent effects of multiple predator species. Oecologia 155, 151159.Google Scholar
Heath, M.R., Speirs, D.C. and Steele, J.H. (2014) Understanding patterns and processes in models of trophic cascades. Ecology Letters 17, 101114.CrossRefGoogle ScholarPubMed
Hegele-Drywa, J. and Normant, M. (2014) Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841) from the southern Baltic Sea. Oceanological and Hydrobiological Studies 43, 219227.CrossRefGoogle Scholar
Hothorn, T., Bretz, K. and Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.CrossRefGoogle ScholarPubMed
Iacarella, J.C., Dick, J.T.A., Alexander, M.E. and Ricciardi, A. (2015) Impacts of aquatic invasive species along temperature gradients: testing the role of environmental matching. Ecology 25, 706716.Google Scholar
Jackson, M.C. (2015) Interactions among multiple invasive animals. Ecology 96, 20352041.Google Scholar
Karsiotis, S.I., Pierce, L.R., Brown, J.E. and Stepien, C.A. (2012) Salinity tolerance of the invasive round goby: experimental implications for seawater ballast exchange and spread to North American estuaries. Journal of Great Lakes Research 38, 121128.Google Scholar
Kidawa, A., Markowska, M. and Rakusa-Suszczewski, S. (2004) Chemosensory behaviour in the mud crab, Rhithropanopeus harrisii tridentatus from Martwa Wisla Estuary (Gdansk Bay, Baltic Sea). Crustaceana 77, 897908.Google Scholar
Kotta, J., Lauringson, V., Martin, G., Simm, M., Kotta, I., Herkül, K. and Ojaveer, H. (2008) Gulf of Riga and Pärnu Bay. In Schiewer, U. (ed.) Ecology of Baltic coastal waters. Ecological Studies 197. Berlin: Springer, pp. 217243.Google Scholar
Kotta, J., Nurkse, K., Puntila, R. and Ojaveer, H. (2016) Shipping and natural environmental conditions determine the distribution of the invasive non-indigenous round goby Neogobius melanostomus in a regional sea. Estuarine, Coastal and Shelf Science 169, 1524.Google Scholar
Kotta, J. and Ojaveer, H. (2012) Rapid establishment of the alien crab Rhithropanopeus harrisii (Gould) in the Gulf of Riga. Estonian Journal of Ecology 61, 293298.Google Scholar
Lee, V.A. and Johnson, T.B. (2005) Development of a bioenergetics model for the round goby (Neogobius melanostomus). Journal of Great Lakes Research 31, 125134.Google Scholar
Lohrer, A.M. and Whitlatch, R.B. (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83, 719732.Google Scholar
Marentette, J.R. and Balshine, S. (2012) Altered prey responses in round goby from contaminated sites. Ethology 118, 812820.CrossRefGoogle Scholar
Newsom, A.J. and Williams, S.L. (2014) Predation and functional responses of Carcinus maenas and Cancer magister in the presence of the introduced Cephalaspidean Philine orientalis . Estuaries and Coasts 37, 12841294.Google Scholar
Nurkse, K., Kotta, J., Orav-Kotta, H. and Ojaveer, H. (2016) A successful non-native predator, round goby, in the Baltic Sea: generalist feeding strategy, diverse diet and high prey consumption. Hydrobiologia 777, 271281.Google Scholar
Nurkse, K., Kotta, J., Orav-Kotta, H., Pärnoja, M. and Kuprijanov, I. (2015) Laboratory analysis of the habitat occupancy of the crab Rhithropanopeus harrisii (Gould) in an invaded ecosystem: the north-eastern Baltic Sea. Estuarine, Coastal and Shelf Science 154, 152157.Google Scholar
Ojaveer, H. (2006) The round goby Neogobius melanostomus is colonising the NE Baltic Sea. Aquatic Invasions 1, 4445.Google Scholar
Ojaveer, H. and Kotta, J. (2015) Ecosystem impacts of the widespread non-indigenous species in the Baltic Sea: literature survey evidences major limitations in knowledge. Hydrobiologia 750, 171185.Google Scholar
Orlova, M.I., Telesh, I.V., Berezina, N.A., Antsulevich, A.E., Maximov, A.A. and Litvinchuk, L.F. (2006) Effects of nonindigenous species on diversity and community functioning in the eastern Gulf of Finland (Baltic Sea). Helgoland Marine Research 60, 98105.Google Scholar
Oyugi, D.O., Cucherousset, J. and Britton, J.R. (2012) Temperature-dependent feeding interactions between two invasive fishes competing through interference and exploitation. Reviews in Fish Biology and Fisheries 22, 499508.Google Scholar
Parker, I.M., Simberloff, D., Lonsdale, W.M., Goodell, K., Wonham, M., Kareiva, P.M., Williamson, M.H., Von Holle, B., Moyle, P.B., Byers, J.E. and Goldwasser, L. (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1, 319.Google Scholar
R Core Team (2016) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Ruiz, G.M., Carlton, J.T., Grosholz, E.D. and Hines, A.H. (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37, 621632.CrossRefGoogle Scholar
Simberloff, D. and Von Holle, B. (1999) Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1, 2132.Google Scholar
Thomsen, M.S., Byers, J.E., Schiel, D.R., Bruno, J.F., Olden, J.D., Wernberg, T. and Silliman, B.R. (2014a) Impacts of marine invaders on biodiversity depend on trophic position and functional similarity. Marine Ecology Progress Series 495, 3947.Google Scholar
Thomsen, M.S., Wernberg, T., Olden, J.D., Byers, J.E., Bruno, J.F., Silliman, B.R. and Schiel, D.R. (2014b) Forty years of experiments on invasive species: are biases limiting our understanding of impacts? Neobiota 22, 122.Google Scholar
Turoboyski, K. (1973) Biology and ecology of the crab Rhithropanopeus harrisii spp. tridentatus . Marine Biology 23, 303313.Google Scholar
Wonham, M.J., O'Connor, M. and Harley, C.D.G. (2005) Positive effects of a dominant invader on introduced and native mudflat species. Marine Ecology Progress Series 289, 109116.Google Scholar