Skip to main content

Advertisement

SpringerLink
Log in

Ecological niche differentiation between native and non-native shrimps in the northern Baltic Sea

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

Invasions of non-native species are modifying global biodiversity but the ecological mechanisms underlying invasion processes are still not well understood. A degree of niche separation of non-native and sympatric native species can possibly explain the success of novel species in their new environment. In this study, we quantified experimentally and in situ the environmental niche space of caridean shrimps (native Crangon crangon and Palaemon adspersus, non-native Palaemon elegans) inhabiting the northern Baltic Sea. Field studies showed that the non-native P. elegans had wider geographical range compared to native species although the level of habitat specialization was similar in both Palaemon species. There were clear differences in shrimp habitat occupancy with P. elegans inhabiting lower salinity areas and more eutrophicated habitats compared to the native species. Consequently, the non-native shrimp has occupied large areas of the northern Baltic Sea that were previously devoid of the native shrimps. Experiments demonstrated that the non-native shrimp had higher affinity to vegetated substrates compared to native species. The study suggests that the abilities of the non-native shrimp to thrive in more stressful habitats (lower salinity, higher eutrophication), that are sub-optimal for native shrimps, plausibly explain the invasion success of P. elegans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguzzi J, Sbragaglia V, Sarriá D, García JA, Costa C, Río JD, Mànuel A, Sardà F (2011) A new laboratory radio frequency identification (RFID) system for behavioural tracking of marine organisms. Sensors 11:9532–9548

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnes RSK (1994) The brackish-water fauna of northwestern Europe: an identification guide to brackish-water habitats, ecology and macrofauna for field-workers, naturalists and students. Cambridge University Press, Cambridge, pp 406–411

    Google Scholar 

  • Bendtsen J, Gustafsson KE, Söderkvist J, Hansen JLS (2009) Ventilation of bottom water in the North Sea-Baltic Sea transition zone. J Mar Syst 75:138–149

    Article  Google Scholar 

  • Berglund A (1980) Niche differentiation between two littoral prawns in Gullmar Fjord, Sweden: Palaemon adspersus and P. squilla. Ecography 3:111–115

    Article  Google Scholar 

  • Berglund A (1981) Sex dimorphism and skewed sex ratios in the prawn species Palaemon adspersus and P. squilla. Oikos 36:158–162

    Article  Google Scholar 

  • Bonsdorff E (2006) Zoobenthic diversity-gradients in the Baltic Sea: continuous post-glacial succession in a stressed ecosystem. J Exp Mar Biol Ecol 330:383–391

    Article  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Castro P, Huber ME (2003) Marine biology, 4th edn. McGraw-Hill, New York, pp 219–221

    Google Scholar 

  • Clavel J, Julliard R, Devictor V (2011) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9:222–228

    Article  Google Scholar 

  • Cuesta JA, González-Ortegón E, Rodríguez A, Baldó F, Vilas C, Drake P (2006) The decapod crustacean community of the Guadalquivir Estuary (SW Spain): seasonal and inter-year changes in community structure. Hydrobiologia 557:85–95

    Article  Google Scholar 

  • Dick JT, Gallagher K, Avlijas S, Clarke HC, Lewis SE, Leung S et al (2013) Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol Invasions 5:837–846

    Article  Google Scholar 

  • Dolédec S, Chessel D, Gimaret-Carpentier C (2000) Niche separation in community analysis: a new method. Ecology 81:2914–2927

    Article  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Duncan RP, Williams PA (2002) Ecology: Darwin’s naturalization hypothesis challenged. Nature 417:608–609

    Article  CAS  PubMed  Google Scholar 

  • Elton CS (1927) The nature and origin of soil-polygons in Spitsbergen. Quarterly Journal of the Geological Society 83:163

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by plants and animals. Methuen, London

    Book  Google Scholar 

  • Eriksson BK, van Sluis Ch, Sieben K, Kautsky L, Råberg S (2010) Omnivory and grazer functional composition moderate cascading trophic effects in experimental Fucus vesiculosus habitats. Mar Biol 158:747–756

    Article  PubMed  PubMed Central  Google Scholar 

  • González-Ortegón E, Pascual E, Cuesta JA, Drake P (2006) Field distribution and osmoregulatory capacity of shrimps in a temperate European estuary (SW Spain). Estuar Coast Shelf Sci 67:293–302

    Article  Google Scholar 

  • Grinnell J (1928) A distributional summation of the ornithology of Lower California. University of California Publications in Zoology 32:1–300

    Google Scholar 

  • Gruszka P, Więcaszek B (2011) Palaemon elegans Rathke, 1837 in the food of Baltic cod (Gadus morhua callarias L., 1758) from the Gulf of Gdańsk. Mar Biol Res 7:100–105

    Article  Google Scholar 

  • Guerin AJ, Neil DM (2015) Escape trajectories of the rockpool prawn (Palaemon elegans) in response to visual and mechanosensory stimuli. Mar Freshw Behav Phy 48:145–161

    Article  Google Scholar 

  • HELCOM (2015) Manual for marine monitoring in the COMBINE programme of HELCOM. http://www.helcom.fi/action-areas/monitoring-and-assessment/manuals-and-guidelines/combine-manual. Accessed February 2016

  • Herkül K, Lauringson V, Kotta J (2016) Specialization among amphipods: the invasive Gammarus tigrinus has narrower niche space compared to native gammarids. Ecosphere. doi:10.1002/ecs2.1306

    Google Scholar 

  • Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA et al (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecol Biogeogr 15:1–7

    Article  Google Scholar 

  • Hubert WA, Pope KL, Dettmers JM (2012) Passive capture techniques. In: Zale AV, Parrish DL, Sutton TM (eds) Fisheries techniques. American Fisheries Society, Bethesda, pp 223–265

    Google Scholar 

  • Janas U, Baranska A (2008) What is the diet of Palaemon elegans Rathe, 1837 (Crustacea, Decapoda), a non-indigenous species in the Gulf of Gdansk (southern Baltic Sea)? Oceanologia 50:221–237

    Google Scholar 

  • Janas U, Mańkucka A (2010) Body size and reproductive traits of Palaemon elegans Rathke, 1837 (Crustacea, Decapoda), a recent colonizer of the Baltic Sea. Oceanol Hydrobiol St 34:3–24

    Google Scholar 

  • Janas U, Piłka M, Lipińska D (2013) Temperature and salinity requirements of Palaemon adspersus Rathke, 1837 and Palaemon elegans Rathke, 1837. Do they explain the occurrence and expansion of prawns in the Baltic Sea? Mar Biol Res 9:293–300

    Article  Google Scholar 

  • Jänes H, Kotta J, Herkül K (2015) High fecundity and predation pressure of the invasive Gammarus tigrinus cause decline of indigenous gammarids. Estuar Coast Shelf Sci 165:185–189

    Article  Google Scholar 

  • Järv L, Kotta J, Raid T (2011) Linking the structure of benthic invertebrate communities and the diet of native and invasive fish species in a brackish water ecosystem. Ann Zool Fenn 48:129–141

    Article  Google Scholar 

  • Katajisto T, Kotta J, Lehtiniemi M, Malavin SA, Panov VE (2013) Palaemon elegans Rathke, 1837 (Caridea: Palaemonoidea: Palaemonidae) established in the Gulf of Finland, the north-eastern Baltic Sea. BioInvasions Records 2:125–132

    Article  Google Scholar 

  • Kotta J, Kuprijanov I (2012) The first finding of the palaemonid shrimp Palaemon elegans Rathke in the Estonian coastal sea. Estonian J Ecol 61:148–153

    Article  Google Scholar 

  • Kotta J, Lauringson V, Martin G, Simm M, Kotta I, Herkül K, Ojaveer H (2008a) Gulf of Riga and Pärnu Bay. In: Schiewer U (ed) Ecology of Baltic coastal waters. Ecological studies, vol 197. Springer, Berlin, pp 217–243

    Chapter  Google Scholar 

  • Kotta J, Paalme T, Püss T, Herkül K, Kotta I (2008b) Contribution of scale-dependent environmental variability on the biomass patterns of drift algae and associated invertebrates in the Gulf of Riga, northern Baltic Sea. J Marine Syst 74:S116–S123

    Article  Google Scholar 

  • Kotta J, Orav-Kotta H, Herkül K (2010) Separate and combined effects of habitat-specific fish predation on the survival of invasive and native gammarids. J Sea Res 64:369–372

    Article  Google Scholar 

  • Kotta J, Orav-Kotta H, Herkül K, Kotta I (2011) Habitat choice of the invasive Gammarus tigrinus and the native Gammarus salinus indicates weak interspecific competition. Boreal Environ Res 16:64–72

    Google Scholar 

  • Kuprijanov I, Kotta J (2013) First evidence on the epiphytic macroalga Pylaiella littoralis on the prawn Palaemon adspersus. Estonian J Ecol 62:287–291

    Article  Google Scholar 

  • Kuprijanov I, Kotta J, Lauringson V, Herkül K (2015) Trophic interactions between native and alien palaemonid prawns and an alien gammarid in a brackish water ecosystem. P Est Acad Sci 64:518–524

    Article  Google Scholar 

  • Łapińska E, Szaniawska A (2005) Seasonal variations in the occurrence of the prawns Crangon crangon (L., 1758), Palaemon adspersus (Rathke, 1837) and Palaemon elegans (Rathke, 1837) in the littoral zone of the Gulf of Gdańsk. Oceanol Hydrobiol St 34:95–110

    Google Scholar 

  • Łapińska E, Szaniawska A (2006) Environmental preferences of Crangon Crangon (Linnaeus, 1758), Palaemon adspersus Rathke, 1837, and Palaemon elegans Rathke, 1837 in the littoral zone of the Gulf of Gdánsk. Crustaceana 79:649–662

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Leibold MA (1995) The niche concept revisited: mechanistic models and community context. Ecology 76:1371–1382

    Article  Google Scholar 

  • Leppäkoski E, Olenin S, Gollasch S (2002) The Baltic Sea—a field laboratory for invasion biology. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe distribution, impacts and management. Springer, Dordrecht, pp 253–259

    Chapter  Google Scholar 

  • Lesutienė J, Gasiūnaitė Z, Strikaitytė R, Žilienė R (2014) Trophic position and basal energy sources of the invasive prawn Palaemon elegans in the exposed littoral of the SE Baltic Sea. Aquat Invasions 9:37–45

    Article  Google Scholar 

  • Ljungberg P, Nilsson PA, Persson A (2012) Prey selectivity by juvenile Atlantic cod Gadus morhua in three coastal habitat types. Mar Ecol Prog Ser 466:215–223

    Article  Google Scholar 

  • Luttikhuizen PC, Campos J, van Bleijswijk J, Peijnenburg KT, van der Veer HW (2008) Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range. Mol Phylogenet Evol 46:1015–1030

    Article  CAS  PubMed  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Maljutenko I, Raudsepp U (2014) Validation of GETM model simulated long-term salinity fields in the pathway of saltwater transport in response to the Major Baltic Inflows in the Baltic Sea. In: Carroll J (ed) 2014 IEEE/OES Baltic International Symposium (BALTIC), IEEE/OES, Tallinn, pp 23–31 http://ieeexplore.ieee.org/lpdocs/epic03/wrapper.htm?arnumber=6887830. Accessed February 2016

  • Marvier M, Kareiva P, Neubert MG (2004) Habitat destruction, fragmentation, and disturbance promote invasion by habitat generalists in a multispecies metapopulation. Risk Anal 24:869–878

    Article  PubMed  Google Scholar 

  • McMahon RF (2002) Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Can J Fish Aquat Sci 59:1235–1244

    Article  Google Scholar 

  • Nikolopoulos A, Isæus M (2008) Wave exposure calculations for the Estonian coast. AquaBiota Water Research, Stockholm, p 26

    Google Scholar 

  • Nurkse K, Kotta J, Orav-Kotta H, Pärnoja M, Kuprijanov I (2015) Laboratory experiment on the habitat occupancy of the crab Rhithropanopeus harrisii (Gould) in an invaded ecosystem: The north-eastern Baltic Sea. Estuar Coast Shelf Sci 154:152–157

    Article  Google Scholar 

  • Oh CW, Hartnoll RG, Nash RD (2001) Feeding ecology of the common shrimp Crangon crangon in Port Erin Bay, Isle of Man, Irish Sea. Mar Ecol Prog Ser 214:211–223

    Article  Google Scholar 

  • Ojaveer H, Kotta J (2015) Ecosystem impacts of the widespread non-indigenous species in the Baltic Sea: literature survey evidences major limitations in knowledge. Hydrobiologia 750:171–185

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan. Accessed February 2016

  • Olenin S, Alemany F, Cardoso AC, Gollasch S, Goulletquer P, Lehtiniemi M, McCollin T, Minchin D, Miossec L, Occhipinti Ambrogi A, Ojaveer H, Jensen KR, Stankiewicz M, Wallentinus I, Aleksandrov B (2010) Marine strategy framework directive—task group 2 report. Office for Official Publications of the European Communities, Non-indigenous species. Luxembourg

    Google Scholar 

  • Pianka ER (1981) Competition and niche theory. In: May RM (ed) Theoretical Ecology, 2nd edn. Blackwell Scientific, Oxford, pp 167–196

    Google Scholar 

  • Pitkänen H, Lehtoranta J, Peltonen H (2008) The Gulf of Finland. In: Schiewer U (ed) Ecology of baltic coastal waters. Ecological studies, vol 197. Springer, Berlin, pp 285–308

    Chapter  Google Scholar 

  • Polechová J, Storch D (2008) Ecological niche. In: Jørgensen SE, Fath BD (eds) Encyclopedia of ecology. Elsevier, Oxford, pp 1088–1097

    Chapter  Google Scholar 

  • Priddis E, Rader R, Belk M, Schaalje B, Merkley S (2009) Can separation along the temperature niche axis promote coexistence between native and invasive species? Divers Distrib 15:682–691

    Article  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed February 2016

  • Reisalu G, Kotta J, Herkül K, Kotta I (2016) The invasive amphipod Gammarus tigrinus Sexton, 1939 displaces native gammarid amphipods from sheltered macrophyte habitats of the Gulf of Riga. Aquat Invasions 11:45–54

    Article  Google Scholar 

  • Reuschel S, Cuesta JA, Schubart CD (2010) Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Mol Phylogenet Evol 55:765–775

    Article  PubMed  Google Scholar 

  • Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282

    Article  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species Invasions: Insights into Ecology, Evolution and Biogeography. Sinauer, Massachusetts, pp 41–64

    Google Scholar 

  • Suursaar Ü, Alari V, Tõnisson H (2014) Multi-scale analysis of wave conditions and coastal changes in the north-eastern Baltic Sea. J Coastal Res 70:223–228

    Article  Google Scholar 

  • Taylor AC, Spicer JI (1987) Metabolic responses of the prawns Palaemon elegans and P. serratus (Crustacea: Decapoda) to acute hypoxia and anoxia. Mar Biol 95:521–530

    Article  CAS  Google Scholar 

  • Weis JS (2011) Invasion and predation in aquatic ecosystems. Curr Zool 57:613–624

    Article  Google Scholar 

  • Zettler ML (2003) Benthologischer Arbeiten zur ökologischen Bewertung von Windenergie-Anlagen-Eignungsgebieten in der Ostsee. Endbericht für die Areale Kriegers Flak (KF) und Westlicher Adlergrund (WAG) Institut für Ostseeforschung, Section für Biologische Meereskunde FKZ:802-85-210, 54 pp

  • Zettler ML, Karlsson A, Kontula T, Gruszka P, Laine AO, Herkül K, Schiele KS, Maximov A, Haldin J (2014) Biodiversity gradient in the Baltic Sea: a comprehensive inventory of macrozoobenthos data. Helgoland Mar Res 68:49–57

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Vitaly Druzhinin for assisting in fieldwork and setting up the experiment; Jelena Kuprijanova and Elisa Ling are thanked for assisting in laboratory analyses. The project has received funding from BONUS Project BIO-C3, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union’s Seventh Programme for research, technological development and demonstration and from the Estonian Research Council. This study was also supported by institutional research funding IUT02-20 of the Estonian Ministry of Education and Research. The targeted field sampling was funded by the Environmental Investment Centre of Estonia in the framework of the Project 2878 SFL nr 3-2_7/31-4/2012 “Identifying an invasive potential of alien shrimp in the Estonian coastal waters”.

Author information

Authors and Affiliations

  1. Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618, Tallinn, Estonia

    Ivan Kuprijanov, Kristjan Herkül & Jonne Kotta

  2. Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia

    Ivan Kuprijanov

  3. School of Natural Sciences and Health, Tallinn University, Narva mnt. 25, 10120, Tallinn, Estonia

    Ivan Kuprijanov

Authors
  1. Ivan Kuprijanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristjan Herkül
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonne Kotta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivan Kuprijanov.

Additional information

Handling Editor: Piet Spaak

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuprijanov, I., Herkül, K. & Kotta, J. Ecological niche differentiation between native and non-native shrimps in the northern Baltic Sea. Aquat Ecol 51, 389–404 (2017). https://doi.org/10.1007/s10452-017-9624-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-017-9624-5

Keywords

Search

Navigation