Skip to main content

Advertisement

SpringerLink
Log in

Different ammonia tolerances may facilitate spatial coexistence of Gammarus roeselii and the strong invader Dikerogammarus villosus

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The introduction of invasive species that can replace native species is one of the most critical threats to the biodiversity of aquatic systems. Here we investigated the potential contribution of one factor to the coexistence of the indigenous amphipod Gammarus roeselii and the invasive amphipod Dikerogammarus villosus in the same ecosystem (Lake Constance) within different microhabitats. We quantitatively studied the influence of ambient ammonia concentrations on the distributions of the two amphipod species. We also assessed the ammonia tolerance ranges of both species in laboratory experiments by measuring mortality rate, precopula disruption, egg mortality, and microhabitat choice. The proportion of G. roeselii among the two amphipod species was significantly positively related to the ammonia concentration in the water, which indicated that the distribution of the invasive D. villosus was limited at high ammonia concentrations. Although the mortality rates of the two species did not significantly differ, G. roeselii was more tolerant to ammonia with regard to precopula disruption, egg mortality, and microhabitat choice. The effective ammonia concentrations that led to a significantly reduced direct reproductive success in D. villosus were within the range of the highest field concentrations measured, where only G. roeselii occurred. D. villosus may have a smaller range than the indigenous G. roeselii partially because of its lower tolerance to higher ammonia concentrations, which lead to reduced reproductive success. Beside other habitat parameters differences on ammonia tolerance between the two amphipods might allow their coexistence along a gradient of microhabitats in Lake Constance.

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

Similar content being viewed by others

References

  • Baumgärtner D, Jungbluth AD, Koch U, von Elert E (2002) Effects of infochemicals on microhabitat choice by the freshwater amphipod Gammarus roeseli. Arch Hydrobiol 155:353–367

    Google Scholar 

  • Bij de Vaate A, Jazdzewski 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 59:1159–1174

    Article  Google Scholar 

  • Brauns M, Garcia X-F, Pusch MT, Walz N (2007) Eulittoral macroinvertebrate communities of lowland lakes: discrimination among trophic states. Freshw Biol 52:1022–1032

    Article  Google Scholar 

  • Bruijs MCM, Kelleher B, van der Velde G, Bij de Vaate A (2001) Oxygen consumption, temperature and salinity tolerance of the invasive amphipod Dikerogammarus villosus: indicators of further dispersal via ballast water transport. Arch Hydrobiol 152:633–646

    Google Scholar 

  • Chandra S, Gerhardt A (2008) Invasive species in aquatic ecosystems: issue of global concern. Aquat Invasions 3:1–2

    Article  Google Scholar 

  • Dick JTA (2008) Role of behaviour in biological invasions and species distributions; lessons from interactions between the invasive Gammarus pulex and the native G. duebeni (Crustacea: Amphipoda). Contrib Zool 77:91–98

    Google Scholar 

  • Dick JTA, Platvoet D (2000) Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proc R Soc Lond Ser B 267:977–983

    Article  CAS  Google Scholar 

  • Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effects of pH and temperature. J Fish Res Board Can 32:2379–2383

    Article  CAS  Google Scholar 

  • Friberg N, Skriver J, Larsen SO, Pedersen ML, Buffagni A (2010) Stream macroinvertebrate occurrence along gradients in organic pollution and eutrophication. Freshw Biol 55:1405–1419

    Article  CAS  Google Scholar 

  • Friedrich G, Pohlmann M (2009) Long-term plankton studies at the lower Rhine/Germany. Limnologica 39:14–39

    Article  CAS  Google Scholar 

  • Gabel F, Pusch MT, Breyer P, Burmester V, Walz N, Garcia X-F (2011) Differential effects of wave stress on the physiology and behaviour of native versus non-native benthic invertebrates. Biol Invasions 13:1843–1853

    Article  Google Scholar 

  • Gergs R, Rothhaupt KO (2008a) Feeding rates, assimilation efficiencies and growth of two amphipod species on biodeposited material from zebra mussels. Freshw Biol 53:2494–2503

    Article  Google Scholar 

  • Gergs R, Rothhaupt KO (2008b) Effects of zebra mussels on a native amphipod and the invasive Dikerogammarus villosus: the influence of biodeposition and structural complexity. J N Am Benthol Soc 27:541–548

    Article  Google Scholar 

  • Gergs R, Grey J, Rothhaupt KO (2011) Temporal variations in zebra mussel (Dreissena polymorpha) density structure the benthic food web and community composition on hard substrates in Lake Constance, Germany. Biol Invasions 13:2727–2738

    Article  Google Scholar 

  • Grabowski M, Bacela K, Konopacka A (2007) How to be an invasive gammarid (Amphipoda: Gammaroidea)—comparison of life history traits. Hydrobiol 590:75–84

    Article  Google Scholar 

  • Hesselschwerdt J, Necker J, Wantzen KM (2008) Gammarids in Lake Constance: habitat segregation between the invasive Dikerogammarus villosus and the indigenous Gammarus roeselii. Fund Appl Limnol 173:177–186

    Article  Google Scholar 

  • Hesselschwerdt J, Tscharner S, Necker J, Wantzen KM (2009) A local gammarid uses kairomones to avoid predation by the invasive crustaceans Dikerogammarus villosus and Orconectes limosus. Biol Invasions 11:2133–2140

    Article  Google Scholar 

  • Kinzler W, Maier G (2003) Asymmetry in mutual predation: possible reason for the replacement of native gammarids by invasives. Arch Hydrobiol 157:473–481

    Article  Google Scholar 

  • Kley A, Maier G (2005) An example of niche partitioning between Dikerogammarus villosus and other invasive and native gammarids: a field study. J Limnol 64:85–88

    Article  Google Scholar 

  • Kley A, Kinzler W, Schank Y, Mayer G, Waloszek D, Maier G (2009) Influence of substrate preference and complexity on co-existence of two non-native gammarideans (Crustacea:Amphipoda). Aquat Ecol 43:1047–1059

    Article  Google Scholar 

  • Lancaster J, Mole A (1999) Interactive effects of near-bed flow and substratum texture on the microdistribution of lotic macroinvertebrates. Arch Hydrobiol 146:83–100

    Google Scholar 

  • Maazouzi C, Masson G, Izquierdo MS, Pihan J-C (2007) Fatty acid composition of the amphipod Dikerogammarus villosus: feeding strategies and trophic links. Comp Biochem Physiol. Part A 147:868–875

    Article  Google Scholar 

  • Maazouzi C, Piscart C, Pihan J-C, Masson G (2009) Effect of habitat-related resources on fatty acid composition and body weight of the invasive Dikerogammarus villosus in an artificial reservoir. Fund Appl Limnol 175:327–338

    Article  CAS  Google Scholar 

  • Maazouzi C, Piscart C, Legier F, Hervant F (2011) Ecophysiological responses to temperature of the “killer shrimp” Dikerogammarus villosus: is the invader really stronger than the native Gammarus pulex? Comp Biochem Physiol A 159:268–274

    Article  CAS  Google Scholar 

  • MacNeil C, Dick JTA, Elwood RW (2000) Differential physico-chemical tolerances of amphipod species revealed by field transformations. Oecologia 124:1–7

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Elwood RW, Montgomery WI (2001a) Coexistence among native and introduced freshwater amphipods (Crustacea); habitat utilization patterns in littoral habitats. Arch Hydrobiol 151:591–607

    Google Scholar 

  • MacNeil C, Montgomery WI, Dick JTA, Elwood RW (2001b) Factors influencing the distribution of native and introduced Gammarus spp. in Irish river systems. Arch Hydrobiol 151:353–368

    Google Scholar 

  • Martens A, Grabow K (2006) The habitat of Crangonyx pseudogracilis in the Upper Rhine region, Germany (Crustacea: Amphipoda): an invasive species is colonizing waters outside the antropogenically influenced main shipping channel. Lauterbornia 58:131–137

    Google Scholar 

  • Mayer G, Maier G, Maas A, Waloszek D (2009) Mouthpart morphology of Gammarus roeselii compared to a successful invader, Dikerogammarus villosus (Amphipoda). J Crustac Biol 29:161–174

    Article  Google Scholar 

  • McCohan CP, Poulton MJ, Thomas PC, Pascoe QXD, Turner C (1991) Lethal and sub-lethal toxicity of field simulated farm waste episodes to several freshwater invertebrate species. Water Res 25:661–671

    Article  Google Scholar 

  • Meijering MPD (1991) Lack of oxygen and low pH as limiting factors for Gammarus in Hessian brooks and rivers. Hydrobiol 223:159–169

    Article  Google Scholar 

  • Mörtl M, Mürle U, Ortlepp J, Rey P, Scheifhacken N, Werner S (2005) Dikerogammarus villosus (Crustacea: Amphipoda) und Corbicula fluminea (Bivalvia: Veneroidea) im Bodensee. In: Baden-Württemberg LfU (ed) Wirbellose Neozoen im Bodensee. Landesanstalt für Umweltschutz Baden-Württemberg, Institut für Seenforschung, Karlsruhe, Germany, pp 15–30

    Google Scholar 

  • Mürle U, Becker A, Rey P (2004) Dikerogammarus villosus (Amphipoda) new in Lake Constance. Lauterbornia 49:77–79

    Google Scholar 

  • Palmer ME, Ricciardi A (2004) Physical factors affecting the relative abundance of native and invasive amphipods in the St. Lawrence River. Can J Zool 82:1886–1893

    Article  Google Scholar 

  • Piscart C, Manach A, Copp GH, Marmonier P (2007) Distribution and microhabitats of native and non-native gammarids (Amphipoda, Crustacea) in Brittany, with particular reference to the endemic sub-species Gammarus duebeni celticus. J Biogeogr 34:524–533

    Article  Google Scholar 

  • Piscart C, Dick JTA, McCrisken D, MacNeil C (2009) Environmental mediation of intraguild predation between the freshwater invader Gammarus pulex and the native G. duebeni celticus. Biol Invasions 11:2141–2145

    Article  Google Scholar 

  • Piscart C, Bergerot B, Laffaille P, Marmonier P (2010) Are amphipod invaders a threat to regional biodiversity? Biol Invasions 12:853–863

    Article  Google Scholar 

  • Piscart C, Kefford BJ, Beiseld JN (2011) Are salinity tolerances of non-native macroinvertebrates in France an indicator of potential for their translocation in a new area? Limnol 41:107–112

    Article  Google Scholar 

  • Platvoet D, Dick JTA, Konijnendijk N, van der Velde G (2006) Feeding on micro-algae in the invasive Ponto-Caspian amphipod Dikerogammarus villosus (Sowinsky, 1894). Aquat Ecol 40:237–245

    Article  Google Scholar 

  • Pöckl M (2007) Strategies of a successful new invader in European freshwaters: fecundity and reproductive potential of the Ponto-Caspian amphipod Dikerogammarus villosus in Austrian Danube, compared with the indigenous Gammarus fossarum and G. roeseli. Freshw Biol 52:50–63

    Article  Google Scholar 

  • Pöckl M, Humpesch UH (1990) Intra- and inter-specific variations in egg survival and brood development time for Austrian populations of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda). Freshw Biol 23:441–455

    Article  Google Scholar 

  • Ponyi E (1956) Ökologische, ernährungsbiologische und systematische Untersuchungen an verschiedenen Gammarus-Arten. Arch Hydrobiol 52:367–387

    Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Riddell GE (2004) Lethal and sublethal toxcicity of ammonia to native, invasive and parasitised freshwater amphipods. Water Res 38:2847–2850

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ricciardi A, MacIsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends Ecol Evol 15:62–65

    Article  PubMed  Google Scholar 

  • Sala OE, Chapin IIFS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oestergeld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global diversity scenarios for the year 2100. Science 287:1770–1774

    Article  PubMed  CAS  Google Scholar 

  • Schulz R, Liess M (1999) A field study of the effects of agriculturally derived insecticide input on stream macroinvertebrate dynamics. Aquat Toxicol 46:155–176

    Article  CAS  Google Scholar 

  • Seager J, Wolff EW, Cooper VA (1988) Proposed environmental quality standards for list II substances in water. Ammonia. WRc report No TR26O

  • Stein S, Bernerth H (2005) Einwanderung gebietsfremder wirbelloser Tiere (Neozoa-Makrozoa) aus hessischen Rhein- und Mainabschnitten in angrenzende Fliessgewässer. In: Albrecht U, Bernerth H, Korte E, Stein S, Tobias W, Wegmann A (eds) Faunistisch-ökologische Untersuchungen des Forschungsinstitutes Senckenberg im hessischen Main. Hessisches Landesamt für Umwelt und Geologie, Wiesbaden, pp 109–167

    Google Scholar 

  • Tittizer T, Schöll F, Banning M, Haybach A, Schleuter M (2000) Aquatische Neozoen im Makrozoobenthos der Binnenwasserstraßen Deutschlands. Lauterbornia 39:1–72

    Google Scholar 

  • Van Riel MC, Van der Velde G, Bij de Vaate A (2009) Interference competition between alien invasive gammaridean species. Biol Invasions 11:2119–2132

    Article  Google Scholar 

  • Wessels M (1998) Geological history of the Lake Constance area. Arch Hydrobiol/Adv Limnol 53:1–12

    Google Scholar 

  • Williams KA, Green DWJ, Pascoe D (1986) Studies on the acute toxicity of pollutants to freshwater macroinvertebrates. Arch Hydrobiol 106:61–70

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Andreas Martens and André Gergs for comments on the manuscript; Melanie Hartwich for help during the field sampling; Jasminca Behrmann-Godel for adopting RG in her working group, which enabled parts of this study; Karen Brune for editing the english language of the manuscript; and Christine Gebauer for ammonium measurements. This study was supported by the Collaborative Research Centre SFB 454 “Littoral of Lake Constance”, the Young Scholar Fund of the University of Konstanz and the research initiative “Internano” at the University of Koblenz-Landau.

Author information

Author notes

  1. René Gergs

    Present address: Institute for Environmental Sciences, University of Koblenz-Landau, 76829, Landau, Germany

Authors and Affiliations

  1. Limnological Institute, University of Konstanz, 78467, Constance, Germany

    René Gergs, Lena Schlag & Karl-Otto Rothhaupt

Authors
  1. René Gergs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lena Schlag
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karl-Otto Rothhaupt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to René Gergs.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gergs, R., Schlag, L. & Rothhaupt, KO. Different ammonia tolerances may facilitate spatial coexistence of Gammarus roeselii and the strong invader Dikerogammarus villosus . Biol Invasions 15, 1783–1793 (2013). https://doi.org/10.1007/s10530-013-0408-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0408-0

Keywords

Search

Navigation