Effect of round goby (Neogobius melanostomus) invasion on blue mussel (Mytilus edulis trossulus) population and winter diet of the long-tailed duck (Clangula hyemalis)

Abstract

The invasive round goby has established a viable population within 9 years of its first introduction to Lithuanian coastal waters (SE Baltic Sea). During its expansion phase, abundances increased 23-fold, which led to the near complete eradication of its main prey, the blue mussel, at < 20 m depth. The round goby population showed a stabilizing trend after blue mussel biomass was depleted; however, their abundance has not declined. The round goby feeds efficiently on newly settled mollusks, causing a severe constraint for blue mussel recovery. Changes in blue mussel availability and size structure induced a dietary shift in wintering long-tailed duck towards fish prey. An energetically dense food source sustains a good body condition in long-tailed ducks, however the change in trophic position (from 3.1 to 4.3 trophic level) suggests the potential for a reduction in their carrying capacity. Results from this study also show that coastal habitats with low and unpredictable population dynamics of blue mussel become less attractive wintering sites for long-tailed duck in the Baltic Sea. We also document a cascading effect of invasive species in the food web.

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References

  1. Andraso GM, Ganger MT, Adamczyk J (2011) Size-selective predation by round gobies (Neogobius melanostomus) on dreissenid mussels in the field. J Great Lakes Res 37(2):298–304

    Article  Google Scholar 

  2. Barret RT, Camphuysen K, Anker-Nilssen T et al (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64(9):1675–1691

    Article  Google Scholar 

  3. Barton DR, Johnson RA, Campbell L, Petruniak J, Patterson M (2005) Effects of round gobies (Neogobius melanostomus) on dreissenid mussels and other invertebrates in eastern Lake Erie, 2002–2004. J Great Lakes Res 31(2):252–261

    Article  Google Scholar 

  4. Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing Ltd., Oxford

    Google Scholar 

  5. Belanger RM, Corkum LD (2003) Susceptibility of tethered round gobies (Neogobius melanostomus) to predation in habitats with and without shelters. J Great Lakes Res 29(4):588–593

    Article  Google Scholar 

  6. Brush AJ, Fisk AT, Hussey NE, Johnson TB (2012) Spatial and seasonal variability in the diet of round goby (Neogobius melanostomus): stable isotopes indicate that stomach contents overestimate the importance of dreissenids. Can J Fish Aquat Sci 69(3):573–586

    Article  CAS  Google Scholar 

  7. Burkett EM, Jude DJ (2015) Long-term impacts of invasive round goby Neogobius melanostomus on fish community diversity and diets in the St. Clair River, Michigan. J Great Lakes Res 41(3):862–872

    Article  Google Scholar 

  8. Bustnes JO, Systad GH (2001) Comparative feeding ecology of Steller’s eider and long-tailed ducks in winter. Waterbirds 24(3):407–412

    Article  Google Scholar 

  9. Cervencl A, Troost K, Dijkman E, de Jong M, Smit CR, Leopold MF, Ens BJ (2015) Distribution of wintering common eider Somateria mollissima in the Dutch Wadden Sea in relation to available food stocks. Mar Biol 162:153–168

    Article  Google Scholar 

  10. Charlebois PM, Marsden JE, Goettel RG, Wolfe RK, Jude DJ, Rudnicka S (1997) The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. Illinois–Indiana Sea Grant Program and Illinois Natural History Survey, Champaign, p 74

    Google Scholar 

  11. Christensen V, Pauly D (1992) ECOPATH II—a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol Model 61:169–185

    Article  Google Scholar 

  12. Crane DP, Farrel JM, Einhouse DW, Lantry JR, Marham JL (2015) Trends in body condition of native piscivores following invasion of Lakes Erie and Ontario by the round goby. Freshw Biol 60:111–124

    Article  Google Scholar 

  13. Dagys M, Švažas S, Žydelis R, Raudonikis L, Vaitkuvienė D (2003) Census of wintering waterfowl. A national report. Institute of Ecology of Vilnius University, Vilnius, Lithuania (in Lithuanian)

  14. Dagys M, Treinys M, Vaitkuvienė D, et al (2013) Investigations of European Commision importance species, invasive midges, ichthyofauna and long distance transfer assessment public purchase—part I. A national report. Institute of Ecology of Vilnius University, Vilnius, Lithuania (in Lithuanian)

  15. Foley CJ, Henebry ML, Happel A et al (2017) Patterns of integration of invasive round goby (Neogobius melanostomus) into a nearshore freshwater food web. Food Webs 10:26–38

    Article  Google Scholar 

  16. French JRP, Jude DJ (2001) Diets and diet overlap of nonidigenous gobies and small benthic native fishes co-inhabiting the St. Clair River, Michigan. J Great Lakes Res 27(3):300–311

    Article  Google Scholar 

  17. Fulton TW (1902) The rate of growth of fishes. 20th Annual Report of the Fishery Board of Scotland 1902(3): 326–446

  18. Ghedotti MJ, Smihula JC, Smith GR (1995) Zebra mussel predation by round gobies in the laboratory. J Great Lakes Res 21(4):665–669

    Article  Google Scholar 

  19. Goss-Custard JD, Stillman RA, Caldow RWG, West AD, Guillemain M (2003) Carrying capacity in overwintering birds: when are spatial models needed? J Appl Ecol 40:176–187

    Article  Google Scholar 

  20. Hearn RD, Harrison AL, Cranswick PA (2015) International single species action plan for the conservation of the long-tailed duck Clangula hyemalis, 2016–2025. AEWA technical series no. 57

  21. HELCOM (2015a) Guidelines for COASTAL FISH monitoring sampling methods of HELCOM, p 25

  22. HELCOM (2015b). Abundance of waterbirds in the wintering season. HELCOM core indicator report. http://www.helcom.fi/Core%20Indicators/Abundance%20of%20waterbirds%20in%20the%20wintering%20season-HELCOM%20core%20indicator%20report%202015-extended%20version.pdf. Accessed 2 Aug 2017

  23. Hempel M, Neukamm R, Thiel R (2016) Effects of introduced round goby (Neogobius melanostomus) on diet composition and growth of zander (Sander lucioperca), a main predator in European brackish waters. Aquat Invasions 11(2):167–178

    Article  Google Scholar 

  24. Hyslop EJ (1980) Stomach content analysis—a review of methods and their application. J Fish Biol 17(4):411–429

    Article  Google Scholar 

  25. Karlson AML, Almqvist G, Skóra KE, Appelberg M (2007) Indications of competition between non-indigenous round goby and native flounder in the Baltic Sea. ICES J Mar Sci 64:479–486

    Article  Google Scholar 

  26. Kautsky N (1982) Quantitative studies on gonad cycle, fecundity, reproductive output and recruitment in a Baltic Mytilus edulis population. Mar Biol 68:143–160

    Article  Google Scholar 

  27. Kornis MS, Mercado-Silva N, Vander Zanden MJ (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80(2):235–285

    Article  PubMed  CAS  Google Scholar 

  28. Kotta J, Nurkse K, Puntila R, Ojaveer H (2016) Shipping and natural environmental conditions determine the distribution of the invasive non-indigenous round goby Neogobius melanostomus in a regional sea. Estuar Coast Shelf Sci 169:15–24

    Article  Google Scholar 

  29. Lauer TE, Allen PH, McComish TS (2004) Changes in mottled sculpin and johnny darter trawl catches after the appearance of round gobies in the Indiana waters of Lake Michigan. Trans Am Fish Soc 133(1):185–189

    Article  Google Scholar 

  30. Lee VA, Johnson TB (2005) Development of a bioenergetics model for the round goby (Neogobius melanostomus). J Great Lakes Res 31:125–134

    Article  Google Scholar 

  31. Linton LR, Davies RW, Wrona FJ (1981) Resource utilization indices: an assessment. J Anim Ecol 50:283–292

    Article  Google Scholar 

  32. Liversage K, Nurkse K, Kotta J, Järv L (2017) Environmental heterogeneity associated with European perch (Perca fluviatilis) predation on invasive round goby (Neogobius melanostomus). Mar Environ Res 132:132–139

    Article  PubMed  CAS  Google Scholar 

  33. Madenjian CP, Stapanian MA, Witzel LD et al (2011) Evidence for predatory control of the invasive round goby. Biol Invasions 13:987–1002

    Article  Google Scholar 

  34. Marchowski D, Neubauer G, Ławicki Ł et al (2015) The importance of non-native prey, the zebra mussel Dreissena polymorpha, for the declining greater scaup Aythya marila: a case study at a key European staging and wintering site. PLoS ONE 10(12):e0145496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Martin FD (1984) Diets of four sympatric species of Etheostoma (Pisces: Percidae) from southern Indiana: interspecific and intraspecific multiple comparisons. Environ Biol Fishes 11(2):113–120

    Article  Google Scholar 

  36. Møller JS, Hansen IS (1994) Hydrographic processes and changes in the Baltic Sea. Dana 10:87–104

    Google Scholar 

  37. Nilsson L (2016) Changes in numbers and distribution of wintering long-tailed ducks Clangula hyemalis in Swedish waters during the last fifty years. Ornis Svecica 26:162–176

    Google Scholar 

  38. Nilsson L, Ogonowski M, Staveley TAB (2016) Factors affecting the local distribution of the long-tailed duck Clangula hyemalis in Baltic offshore waters. Wildfowl 66:142–158

    Google Scholar 

  39. Nurkse Kotta J, Orav-Kotta H, 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(1):271–281

    Article  CAS  Google Scholar 

  40. Oesterwind D, Bock C, Förster A et al (2017) Predator and prey: the role of the round goby Neogobius melanostomus in the western Baltic. Mar Biol Res 13(2):188–197

    Article  Google Scholar 

  41. Ojaveer H, Galil B, Lehtiniemi M et al (2015) Twenty five years of invasion: management of the round goby Neogobius melanostomus in the Baltic Sea. Manag Biol Invasion 6(4):329–339

    Article  Google Scholar 

  42. Olenin S, Daunys D (2004) Coastal typology based on benthic biotope and community data: the Lithuanian case study. Coastline Rep 4:65–83

    Google Scholar 

  43. Olenin S, Gollasch S, Lehtiniemi M, Sapota M, Zaiko A (2017) Biological invasions. In: Snoeijs-Leijonmalm P, Schubert H, Radziejewska T (eds) Biological oceanography of the Baltic Sea. Springer, Dordrecht, pp 193–232

    Google Scholar 

  44. Pennuto CM, Krakowiak PJ, Janik CE (2010) Seasonal abundance, diet, and energy consumption of round gobies (Neogobius melanostomus) in Lake Erie tributary streams. Ecol Freshw Fish 19(2):206–215

    Article  Google Scholar 

  45. Raudonikis L, Sorokaitė L (2010) Condition assessment of European Commision importance bird species with a demand to establish protected areas. A national report. Institute of Ecology of Vilnius University, Vilnius, Lithuania (in Lithuanian)

  46. Ray WJ, Corkum LD (2001) Habitat and site affinity of the round goby. J Great Lakes Res 27(3):329–334

    Article  Google Scholar 

  47. Razinkovas-Baziukas A, Morkūnė R, Bacevičius E, Gasiūnaitė ZR (2017) Trophic network model of exposed sandy coast: linking continental and marine water ecosystems. Estuar Coast Shelf Sci 195:110–123

    Article  Google Scholar 

  48. Reid SM, Mandrak NE (2008) Historical changes in the distribution of threatened channel darter (Percina copelandi) in Lake Erie with general observations on the beach fish assemblage. J Great Lakes Res 34(2):324–333

    Article  Google Scholar 

  49. Rumohr H, Brey T, Ankar S (1987) A compilation of biometrics conversion factors for benthic invertebrates of the Baltic Sea. Baltic Marine Biologists Publication No. 9

  50. Samuilovienė A, Jonsson PR, Šiaulys A, Kotta J, Zaiko A (in prep) Connectivity profiles of temperate reef habitats for guiding adaptive conservation strategies in the context of changing marine ecosystem

  51. Sapota MR, Skóra KE (2005) Spread of alien (non-indigenous) fish species Neogobius melanostomus in the Gulf of Gdansk (south Baltic). Biol Invasions 7:157–164

    Article  Google Scholar 

  52. Schoener TW (1970) Non-synchronous spatial overlap of lizards in patchy environments. Ecology 51(3):408–418

    Article  Google Scholar 

  53. Schrandt MN, Stone LC, Klimek B, Mäkelin S, Heck KL, Matilla J, Herlevi H (2016) A laboratory study of potential effects of the invasive round goby on nearshore fauna of the Baltic Sea. Aquat Invasions 11(3):327–335

    Article  Google Scholar 

  54. Schummer ML, Petrie SA, Bailey RC (2008) Dietary overlap of sympatric diving ducks during winter on northeastern Lake Ontario. Auk 125(2):425–433

    Article  Google Scholar 

  55. Simonović P, Paunović M, Popović S (2001) Morphology, feeding, and reproduction of the round goby, Neogobiusmelanostomus (Pallas), in the Danube River basin, Yugoslavia. J Great Lakes Res 27(3):281–289

    Article  Google Scholar 

  56. Skabeikis A, Lesutienė J (2015) Feeding activity and diet composition of round goby (Neogobius melanostomus, Pallas 1814) in the coastal waters of SE Baltic Sea. Oceanol Hydrobiol Stud 44(4):508–519

    Article  CAS  Google Scholar 

  57. Skóra K, Rzeznik J (2001) Observations on diet composition of Neogobius melanostomus Pallas 1811 (Gobiidae, Pisces) in the Gulf of Gdańsk (Baltic Sea). J Great Lakes Res 27(3):290–299

    Article  Google Scholar 

  58. Skov H, Heinänen S, Žydelis R, et al (2011) Waterbird populations and pressures in the Baltic Sea. Tema Nord, p 550

  59. Steimle FW, Terranova RJ (1985) Energy equivalents of marine organisms from the continental shelf of the temperate Northwest Atlantic. J Northwest Atl Fish Sci 6:117–124

    Article  Google Scholar 

  60. Stempniewicz L (1995) Feeding ecology of the long-tailed duck Clangula hyemalis wintering in the Gulf of Gdańsk (southern Baltic Sea). Ornis Svecica 5:133–142

    Google Scholar 

  61. Taraborelli AC, Schaner T (2002) Diet of round goby in the bay of Quinte, Lake Ontario. Lake Ontario communities and fisheries: 2001 annual report of the Lake Onterio management unit: 106–109

  62. The IUCN red list of threatened species. Version 2016-3. http://www.iucnredlist.org/. Accessed 3 May 2017

  63. Thompson HA, Simon TP (2014) Diet shift response in round goby, Neogobius melanostomus, based on size, sex, depth and habitat in the western basin of Lake Erie. J Appl Ichthyol 30(5):955–961

    Article  Google Scholar 

  64. Ustups D, Bergström U, Florin AB, Kruze E, Zilniece D, Elferts D, Knospina E, Uzars D (2016) Diet overlap between juvenile flatfish and the invasive round goby in the central Baltic Sea. J Sea Res 107(1):121–129

    Article  Google Scholar 

  65. van Franeker JA (2004) Save the North Sea Fulmar-Litter-EcoQO manual part 1: collection and dissection procedures. Wageningen, Alterra, Alterra-rapport 672

  66. van Kessel N, Dorenbosch M, Kranenbarg J, van der Velde G, Leuwen RSEW (2016) Invasive Ponto-Caspian gobies rapidly reduce the abundance of protected native bullhead. Aquat Invasions 11(2):179–188

    Article  Google Scholar 

  67. Waldeck P, Larsson K (2013) Effects of winter water temperature on mass loss in Baltic blue mussels: implications for foraging sea ducks. J Exp Mar Biol Ecol 444:24–30

    Article  Google Scholar 

  68. Werner EE, Hall DJ (1974) Optimal foraging and size selection of prey by bluegill sunfish (Lepomis macrochirus). Ecology 55:1042–1052

    Article  Google Scholar 

  69. Zolubas T (2003) New invasive fish species in Lithuanian waters. Jūra ir aplinka 2(9):52–56 (in Lithuanian)

    Google Scholar 

  70. Žydelis R (1997) Preliminary study of Steller’s eider Polysticta stelleri ecology at Palanga coast, Eastern Baltic. Acta Zool Litu 6(1):107–111

    Article  Google Scholar 

  71. Žydelis R (2002) Habitat selection of the waterbirds wintering in the Lithuanian coastal zone of the Baltic Sea. Dissertation, Vilnius University

  72. Žydelis R, Švažas S, Dagys M, Raudonikis L (2002) Census of wintering waterfowl. A national report. Institute of Ecology of Vilnius University, Vilnius, Lithuania (in Lithuanian)

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Acknowledgements

We thank the fisheries service under the Ministry of Agriculture of the Republic of Lithuania, Division of Fishery Research and Science for long-term round goby abundance data. We also thank commercial fishermen, who provided long-tailed ducks caught in their gill nets, and undergraduate students for help during laboratory analysis of the bird diet. We thank dr. A. Petraitis for long-tailed duck diet data from 2002 to 2004 and volunteers from the Lithuanian Ornithological Society for mid-winter bird counts. We also thank prof. S. Olenin, prof. D. Daunys, dr. M. Bučas, and dr. A. Šaškov for blue mussel sampling, S. Karalius for drawing and prof. P. Bukaveckas for language revision. This study was supported by BIO-C3 (Biodiversity changes-causes, consequences and management implications) within BONUS, the joint Baltic Sea Research and Development program funded jointly by the EU Seventh Framework Programme and the Research Council of Lithuania (Grant Agreement No. BONUS-1/2014).

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Skabeikis, A., Morkūnė, R., Bacevičius, E. et al. Effect of round goby (Neogobius melanostomus) invasion on blue mussel (Mytilus edulis trossulus) population and winter diet of the long-tailed duck (Clangula hyemalis). Biol Invasions 21, 911–923 (2019). https://doi.org/10.1007/s10530-018-1869-y

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Keywords

  • Resource competition
  • Trophic level
  • Marine protected area