Advertisement

Aquatic Ecology

, Volume 52, Issue 2–3, pp 179–190 | Cite as

Niche differentiation among invasive Ponto-Caspian Chelicorophium species (Crustacea, Amphipoda, Corophiidae) by food particle size

  • Péter Borza
  • Thomas Huber
  • Patrick Leitner
  • Nadine Remund
  • Wolfram Graf
Article
First Online:
Received:
Accepted:

Abstract

After Chelicorophium curvispinum, two other Ponto-Caspian tube-dwelling, filter-feeding amphipod species (Chelicorophium robustum and Chelicorophium sowinskyi) have colonized several catchments in Central and Western Europe in recent decades. To reveal the mechanism of niche differentiation among them, we measured the mesh sizes of their filtering apparatus and analyzed multi-habitat sampling data from the River Danube using RDA-based variance partitioning between environmental and spatial explanatory variables. Morphometric data showed a clear differentiation among the species by filter mesh size (C. curvispinum > C. robustum > C. sowinskyi). Field data also indicated the relevance of suspended matter; however, the mere quantity of suspended solids included in the analysis could not explain the abundance patterns effectively. Current velocity, substrate types, and total nitrogen content also had a non-negligible effect; however, their role in the niche differentiation of the species is not evident. In summary, differences in their filter mesh sizes indicate a niche differentiation by food particle size among the invasive Chelicorophium species, allowing their stable coexistence given sufficient size variability in their food source. Consequently, the two recent invaders increase the effectiveness of resource utilization, resulting in a more intensive benthic–pelagic coupling in the colonized ecosystems.

Keywords

Benthic–pelagic coupling Filter-feeding Invasion impact River Danube Suspended matter 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Joint Danube Survey 3 was organized by the International Commission for the Protection of the Danube River (ICPDR). We would like to thank everyone involved in the organization, field work, and evaluation of the survey for their effort, and Zsuzsanna Trábert for her assistance during the microscopy. This work was supported by the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded by the European Union under the 7th Framework Programme, grant agreement no: 603378, and the Economic Development and Innovation Operational Programme (GINOP) 2.3.2-15-2016-00019 grant. Péter Borza was supported by the Scholarship of the Scholarship Foundation of the Republic of Austria for Post-docs from October 2013 until March 2014 (funding organization: Österreichischer Austauschdienst GmbH on behalf of and financed by the Scholarship Foundation of the Republic of Austria).

Supplementary material

10452_2018_9653_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 28 kb)

References

  1. Altermatt F, Alther R, Fišer C, Jokela J, Konec M, Küry D, Mächler E, Stucki P, Westram AM (2014) Diversity and distribution of freshwater amphipod species in Switzerland (Crustacea: Amphipoda). PLoS ONE 9:e110328CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atkinson CL, Vaughn CC, Forshay KJ, Cooper JT (2013) Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology 94:1359–1369CrossRefPubMedGoogle Scholar
  3. Bernauer D, Jansen W (2006) Recent invasions of alien macroinvertebrates and loss of native species in the upper Rhine River, Germany. Aquat Invasions 1:55–71CrossRefGoogle Scholar
  4. Bernerth H, Dorow S (2010) Chelicorophium sowinskyi (Crustacea, Amphipoda) ist aus der Donau in den Main vorgedrungen - Anmerkungen zur Verbreitung und Morphologie der Art. Lauterbornia 70:53–71Google Scholar
  5. Bernerth H, Tobias W, Stein S (2005) Faunenwandel im Main zwischen 1997 und 2002 am Beispiel des Makrozoobenthos. Faunistisch-ökologische Untersuchungen des Forschungsinstitutes Senckenberg im hessischen Main. Hessisches Landesamt für Umwelt und Geologie, Wiesbaden, pp 15–87Google Scholar
  6. Bij de Vaate A, Jażdżewski K, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174CrossRefGoogle Scholar
  7. Blanchet FG, Legendre P, Borcard D (2008a) Modelling directional spatial processes in ecological data. Ecol Model 215:325–336CrossRefGoogle Scholar
  8. Blanchet FG, Legendre P, Borcard D (2008b) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefPubMedGoogle Scholar
  9. Blanchet FG, Legendre P, Maranger R, Monti D, Pepin P (2011) Modelling the effect of directional spatial ecological processes at different scales. Oecologia 166:357–368CrossRefPubMedGoogle Scholar
  10. Borza P (2011) Revision of invasion history, distributional patterns, and new records of Corophiidae (Crustacea: Amphipoda) in Hungary. Acta Zool Acad Sci Hung 57:75–84Google Scholar
  11. Borza P, Csányi B, Paunović M (2010) Corophiids (Amphipoda, Corophioidea) of the River Danube the results of a longitudinal survey. Crustaceana 83:839–849CrossRefGoogle Scholar
  12. Borza P, Csányi B, Huber T, Leitner P, Paunović M, Remund N, Szekeres J, Graf W (2015) Longitudinal distributional patterns of Peracarida (Crustacea, Malacostraca) in the River Danube. Fundam Appl Limnol 187:113–126CrossRefGoogle Scholar
  13. Borza P, Huber T, Leitner P, Remund N, Graf W (2017a) Current velocity shapes co-existence patterns among invasive Dikerogammarus species. Freshw Biol 62:317–328CrossRefGoogle Scholar
  14. Borza P, Huber T, Leitner P, Remund N, Graf W (2017b) Success factors and future prospects of Ponto-Caspian peracarid (Crustacea: Malacostraca) invasions: Is “the worst over”? Biol Invasions 19:1517–1532CrossRefGoogle Scholar
  15. Brönmark C, Malmqvist B (1982) Resource partitioning between unionid mussels in a Swedish lake outlet. Ecography 5:389–395CrossRefGoogle Scholar
  16. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  17. Cheer AYL, Koehl MAR (1987) Paddles and rakes: fluid flow through bristled appendages of small organisms. J Theor Biol 129:17–39CrossRefGoogle Scholar
  18. Dokulil MT, Donabaum U (2014) Phytoplankton of the Danube river: composition and long-term dynamics. Acta Zool Bulg Suppl 7:147–152Google Scholar
  19. Fenchel T, Kofoed LH, Lappalainen A (1975) Particle size-selection of two deposit feeders: the amphipod Corophium volutator and the prosobranch Hydrobia ulvae. Mar Biol 30:119–128CrossRefGoogle Scholar
  20. Forcellini M (2012) First record of the Ponto-Caspian invasive crustacean Chelicorophium sowinskyi (Martinov, 1924) (Amphipoda, Corophiidae) in the French Rhône River. Crustaceana 85:1781–1785CrossRefGoogle Scholar
  21. Griffiths JR, Kadin M, Nascimento FJA, Tamelander T, Törnroos A, Bonaglia S, Bonsdorff E, Brüchert V, Gårdmark A, Järnström M, Kotta J, Lindegren M, Nordström MC, Norkko A, Olsson J, Weigel B, Žydelis R, Blenckner T, Niiranen S, Winder M (2017) The importance of benthic-pelagic coupling for marine ecosystem functioning in a changing world. Glob Change Biol 23:2179–2196CrossRefGoogle Scholar
  22. Hellmann C, Worischka S, Mehler E, Becker J, Gergs R, Winkelmann C (2015) The trophic function of Dikerogammarus villosus (Sowinsky, 1894) in invaded rivers: a case study in the Elbe and Rhine. Aquat Invasions 10:385–397CrossRefGoogle Scholar
  23. Hering D, Moog O, Sandin L, Verdonschot PF (2004) Overview and application of the AQEM assessment system. Hydrobiologia 516:1–20CrossRefGoogle Scholar
  24. Higgins SN, Vander Zanden MJ (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecol Monogr 80:179–196CrossRefGoogle Scholar
  25. Jones LA, Ricciardi A (2005) Influence of physicochemical factors on the distribution and biomass of invasive mussels (Dreissena polymorpha and Dreissena bugensis) in the St. Lawrence River. Can J Fish Aquat Sci 62:1953–1962CrossRefGoogle Scholar
  26. Kang C-K, Choy EJ, Hur Y-B, Myeong J-I (2009) Isotopic evidence of particle size-dependent food partitioning in cocultured sea squirt Halocynthia roretzi and Pacific oyster Crassostrea gigas. Aquat Biol 6:289–302CrossRefGoogle Scholar
  27. Kelleher B, Bergers PJM, Van den Brink FWB, Giller PS, Van der Velde G, Bij de Vaate A (1998) Effects of exotic amphipod invasions on fish diet in the Lower Rhine. Arch Für Hydrobiol 143:363–382CrossRefGoogle Scholar
  28. Labat F, Piscart C, Fontan B (2011) First records, pathways and distributions of four new Ponto-Caspian amphipods in France. Limnologica 41:290–295CrossRefGoogle Scholar
  29. Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579CrossRefGoogle Scholar
  30. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefPubMedGoogle Scholar
  31. Legendre P, Legendre LF (2012) Numerical ecology, 3rd English edition edn. Elsevier, AmsterdamGoogle Scholar
  32. Lesser MP, Shumway SE, Cucci T, Smith J (1992) Impact of fouling organisms on mussel rope culture: interspecific competition for food among suspension-feeding invertebrates. J Exp Mar Biol Ecol 165:91–102CrossRefGoogle Scholar
  33. Møller LF, Riisgård HU (2006) Filter feeding in the burrowing amphipod Corophium volutator. Mar Ecol Prog Ser 322:213–224CrossRefGoogle Scholar
  34. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  35. Noordhuis R, van Schie J, Jaarsma N (2009) Colonization patterns and impacts of the invasive amphipods Chelicorophium curvispinum and Dikerogammarus villosus in the IJsselmeer area, The Netherlands. Biol Invasions 11:2067–2084CrossRefGoogle Scholar
  36. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2017) Vegan: Community Ecology Package. R package version 2.4-3. http://CRAN.R-project.org/package=vegan
  37. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-125, http://CRAN.R-project.org/package=nlme
  38. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  39. Riisgård HU, Larsen PS (2010) Particle capture mechanisms in suspension-feeding invertebrates. Mar Ecol Prog Ser 418:255–293CrossRefGoogle Scholar
  40. Rohlf FJ (2015) tpsDig, Digitize Landmarks and Outlines, version 2.22. Department of Ecology and Evolution, State University of New York, Stony BrookGoogle Scholar
  41. Shimeta J, Jumars PA (1991) Physical mechanisms and rates of particle capture by suspension-feeders. Oceanogr Mar Biol Annu Rev 29:l–257Google Scholar
  42. Sousa R, Novais A, Costa R, Strayer DL (2014) Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735:233–251CrossRefGoogle Scholar
  43. Svensson JR, Marshall DJ (2015) Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space. Ecology 96:819–827CrossRefPubMedGoogle Scholar
  44. Van den Brink FWB, Van der Velde G, Bij de Vaate A (1993) Ecological aspects, explosive range extension and impact of a mass invader, Corophium curvispinum Sars, 1895 (Crustacea: Amphipoda), in the Lower Rhine (The Netherlands). Oecologia 93:224–232CrossRefPubMedGoogle Scholar
  45. Van der Velde G, Paffen BGP, Van den Brink FWB, Bij de Vaate A, Jenner HA (1994) Decline of zebra mussel populations in the Rhine. Naturwissenschaften 81:32–34CrossRefGoogle Scholar
  46. Van Riel MC, Van der Velde G, Rajagopal S, Marguillier S, Dehairs F, Bij de Vaate A (2006) Trophic relationships in the Rhine food web during invasion and after establishment of the Ponto-Caspian invader Dikerogammarus villosus. Hydrobiologia 565:39–58CrossRefGoogle Scholar
  47. Wallace JB, Webster JR, Woodall WR (1977) The role of filter feeders in flowing waters. Arch Für Hydrobiol 79:506–532Google Scholar
  48. Zhang X, Liu Z, Jeppesen E, Taylor WD, Rudstam LG (2016) Effects of benthic-feeding common carp and filter-feeding silver carp on benthic-pelagic coupling: implications for shallow lake management. Ecol Eng 88:256–264CrossRefGoogle Scholar
  49. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.GINOP Sustainable Ecosystems GroupMTA Centre for Ecological ResearchTihanyHungary
  2. 2.Danube Research InstituteMTA Centre for Ecological ResearchBudapestHungary
  3. 3.Department of Water, Atmosphere and Environment, Institute for Hydrobiology and Water ManagementBOKU - University of Natural Resources and Applied Life SciencesViennaAustria
  4. 4.Info fauna – CSCFNeuchâtelSwitzerland

Personalised recommendations

Cite article

Buy options