Skip to main content
Log in

The effectiveness of the induced anti-predator behaviour of zebra mussel Dreissena polymorpha in the presence of molluscivorous roach Rutilus rutilus

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

We checked whether the induced anti-predator defences of zebra mussels are able to affect the predation success of roach, being one of the most efficient zebra mussel predators in Europe. Previously, several anti-predator defences of mussels have been observed in the presence of roach, including stronger attachment, aggregation forming and inhibition of upward movement. However, the actual efficiency of these responses to reduce the mussel vulnerability to predation was unknown. To check the effectiveness of attachment strength, we exposed mussels for 6 (strong attachment), 1 (weak attachment) or 0 (unattached) days in ceramic trays and then presented the trays to fish in an experimental tank. To test the effectiveness of aggregation, we glued mussels to the trays in groups of three (touching one another) or singly using denture glue and exposed them to fish. To check the effect of the vertical position, we glued mussels with denture glue to the bottom and 10, 20 and 30 cm above the bottom of the tank with fish. After 1-h exposure, we determined the percentages of consumed mussels. Roach predation rate was lowest on strongly attached mussels, intermediate on weakly attached mussels and highest on unattached mussels. Aggregated mussels were less frequently consumed than singletons. Conversely, the vertical position of mussels did not affect the roach predation success. Our study demonstrates that the behavioural defences exhibited by zebra mussels can increase their survival in the presence of predators and thus emphasizes the importance of the anti-predator behaviour of this species.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Burks RL, Tuchman NC, Call CA, Marsden JE (2002) Colonial aggregates: effects of spatial position on zebra mussel responses to vertical gradients in interstitial water quality. J N Am Benthol Soc 21:64–75

    Article  Google Scholar 

  • Caro AU, Castilla JC (2004) Predator-inducible defences and local intra-population variability of the intertidal mussel Semimytilus algosus in central Chile. Mar Ecol Prog Ser 276:115–123

    Article  Google Scholar 

  • Chase ME, Bailey RC (1996) Recruitment of Dreissena polymorpha: does the presence and density of conspecifics determine the recruitment density and pattern in a population? Malacologia 38:19–31

    Google Scholar 

  • Cheung SG, Tong PY, Yip KM, Shin PKS (2004) Chemical cues from predators and damaged conspecifics affect byssus production in the green-lipped mussel Perna viridis. Mar Freshwat Behav Physiol 37:127–135

    Article  CAS  Google Scholar 

  • Cheung SG, Luk KC, Shin PKS (2006) Predator-labeling effect on byssus production in marine mussels Perna viridis (L.) and Brachidontes variabilis (Krauss). J Chem Ecol 32:1501–1512

    Article  PubMed  CAS  Google Scholar 

  • Côté IM, Jelnikar E (1999) Predator-induced clumping behaviour in mussels (Mytilus edulis Linnaeus). J Exp Mar Biol Ecol 235:201–211

    Article  Google Scholar 

  • Czarnołęski M, Kozłowski J, Kubajak P, Lewandowski K, Müller T, Stańczykowska A, Surówka K (2006) Cross-habitat differences in crush resistance and growth pattern of zebra mussels (Dreissena polymorpha): effects of calcium availability and predator pressure. Arch Hydrobiol 165:191–208

    Article  Google Scholar 

  • Czarnołęski M, Müller T, Adamus K, Ogorzelska G, Sog M (2010) Injured conspecifics alter mobility and byssus production in zebra mussels Dreissena polymorpha. Fundam Appl Limnol 176:269–278

    Article  Google Scholar 

  • De Meester L, Weider LJ (1999) Depth selection behavior, fish kairomones and the life histories of Daphnia hyalina x galeata hybrid clones. Limnol Oceanogr 44:1248–1258

    Article  Google Scholar 

  • De Meester L, Dawidowicz P, Van Gool E, Loose CJ (1999) Ecology and evolution of predator-induced behavior of zooplankton: depth selection behavior and diel vertical migration. In: Tollrian R, Harvel CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 160–176

    Google Scholar 

  • Dzialowski AR, Lennon JT, O’Brien WJ, Smith VH (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshwat Biol 48:1593–1602

    Article  Google Scholar 

  • Farrell ED, Crowe TP (2007) The use of byssus threads by Mytilus edulis as an active defence against Nucella lapillus. J Mar Biol Assoc UK 87:559–564

    Article  Google Scholar 

  • Freeman AS (2007) Specificity of induced defenses in Mytilus edulis and asymmetrical predator deterrence. Mar Ecol Prog Ser 334:145–153

    Article  Google Scholar 

  • Gliwicz ZM (2005) Food web interactions: why are they reluctant to be manipulated? Plenary Lecture. Verh Internat Verein Limnol 29:73–88

    Google Scholar 

  • Gosling E (2003) Bivalve molluscs. Biology, ecology and culture. Fishing News Books, Blackwell Publishing, Oxford

  • Green NS, Hazlett BA, Prueff-Jones S (2008) Attachment and shell integrity affects the vulnerability of zebra mussels (Dreissena polymorpha) to predation. J Freshwat Ecol 23:91–99

    Article  Google Scholar 

  • Hawkins AKS, Bayne BL (1985) Seasonal variation in the relative utilization of carbon and nitrogen by the mussel Mytilus edulis: budgets, conversion efficiencies and maintenance requirements. Mar Ecol Prog Ser 25:181–188

    Article  CAS  Google Scholar 

  • Heller R, Milinski M (1979) Optimal foraging of sticklebacks on swarming prey. Anim Behav 27:1127–1141

    Article  Google Scholar 

  • Hoverman JT, Relyea RA (2009) Survival trade-offs associated with inducible defences in snails: the roles of multiple predators and developmental plasticity. Funct Ecol 23:1179–1188

    Article  Google Scholar 

  • Ishida S, Iwasaki K (2003) Reduced byssal thread production and movement by the intertidal mussel Hormomya mutabilis in response to effluent from predators. J Ethol 21:117–122

    Google Scholar 

  • Kobak J (2006a) Geotactic behaviour of Dreissena polymorpha (Bivalvia). Malacologia 48:305–308

    Google Scholar 

  • Kobak J (2006b) Factors influencing the attachment strength of Dreissena polymorpha (Bivalvia). Biofouling 22:153–162

    Article  PubMed  Google Scholar 

  • Kobak J, Kakareko T (2009) Attachment strength, aggregation and movement of the zebra mussel (Dreissena polymorpha, Bivalvia) in the presence of potential predators. Fundam Appl Limnol 174:193–204

    Article  Google Scholar 

  • Kobak J, Nowacki P (2007) Light-related behaviour of zebra mussel (Dreissena polymorpha, Bivalvia). Fundam Appl Limnol 169:341–352

    Article  Google Scholar 

  • Kobak J, Kakareko T, Poznańska M (2010) Changes in attachment strength and aggregation of zebra mussel, Dreissena polymorpha in the presence of potential fish predators of various species and size. Hydrobiologia 644:195–206

    Article  Google Scholar 

  • Koperski P (1997) Changes in feeding behaviour of the larvae of the damselfly Enallagma cyathigerum in response to stimuli from predators. Ecol Entomol 22:167–175

    Article  Google Scholar 

  • Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239

    Article  Google Scholar 

  • Magurran AE (1990) The adaptive significance of schooling as an antipredator defence in fish. Ann Zool Fenn 27:51–66

    Google Scholar 

  • Molloy DP, Karatayev AY, Burlakova LE, Kurandina DP, Laruelle F (1997) Natural enemies of zebra mussels: predators, parasites, and ecological competitors. Rev Fish Sci 5:27–97

    Article  Google Scholar 

  • Naddafi R, Eklöv P, Pettersson K (2007) Non-lethal predator effects on the feeding rate and prey selection of the exotic zebra mussel Dreissena polymorpha. Oikos 116:1289–1298

    Article  Google Scholar 

  • Naddafi R, Pettersson K, Eklöv P (2010) Predation and physical environment structure the density and population size structure of zebra mussels. J N Am Benthol Soc 29:444–453

    Article  Google Scholar 

  • Nagelkerke LAJ, Sibbing FA (1996) Efficiency of feeding on zebra mussel (Dreissena polymorpha) by common bream (Abramis brama), white bream (Blicca bjoerkna), and roach (Rutilus rutilus): the effects of morphology and behavior. Can J Fish Aquat Sci 53:2847–2861

    Article  Google Scholar 

  • Pettersson LB, Nilsson PA, Brönmark C (2000) Predator recognition and defence strategies in crucian carp, Carassius carassius. Oikos 88:200–212

    Article  Google Scholar 

  • Pijanowska J, Kowalczewski A (1997) Predators can induce swarming behaviour and locomotory responses in Daphnia. Freshwat Biol 37:649–656

    Article  Google Scholar 

  • Prejs A, Lewandowski K, Stańczykowska A (1990) Size-selective predation by roach (Rutilus rutilus) on zebra mussel (Dreissena polymorpha): field studies. Oecologia 83:378–384

    Google Scholar 

  • Reimer O, Harms-Ringdahl S (2001) Predator-inducible changes in blue mussels from the predator-free Baltic Sea. Mar Biol 139:959–965

    Article  Google Scholar 

  • Reimer O, Tedengren M (1996) Phenotypical improvement of morphological defences in the mussel Mytilus edulis induced by exposure to the predator Asterias rubens. Oikos 75:383–390

    Article  Google Scholar 

  • Reimer O, Tedengren M (1997) Predator-induced changes in byssal attachment, aggregation and migration in the blue mussel, Mytilus edulis. Mar Freshwat Behav Physiol 30:251–266

    Article  Google Scholar 

  • Smallegange IM, Van Der Meer J (2003) Why do shore crabs not prefer the most profitable mussels? J Anim Ecol 72:599–607

    Article  Google Scholar 

  • Stańczykowska A (1964) On the relationship between abundance, aggregations and “condition” of Dreissena polymorpha Pall. in 36 Mazurian Lakes. Ekol Pol A 34:653–690

    Google Scholar 

  • Tollrian R (1995) Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia 101:151–155

    Article  Google Scholar 

  • Toomey MB, McCabe D, Marsden JE (2002) Factors affecting the movement of adult zebra mussels (Dreissena polymorpha). J N Am Benthol Soc 21:468–475

    Article  Google Scholar 

  • Tuchman NC, Burks RL, Call CA, Smarrelli J (2004) Flow rate and vertical position influence ingestion rates of colonial zebra mussels (Dreissena polymorpha). Freshwat Biol 49:191–198

    Article  Google Scholar 

  • Van Buskirk J, McCollum SA (2000) Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation. J Evol Biol 13:336–347

    Article  Google Scholar 

  • Wiąckowski K, Fyda J, Ciećko A (2004) The behaviour of an omnivorous protozoan affects the extent of induced morphological defence in a protozoan prey. Freshwat Biol 49:801–809

    Article  Google Scholar 

  • Wiltshire KH, Lampert W (1999) Urea excretion by Daphnia: a colony-inducing factor in Scenedesmus? Limnol Oceanogr 44:1894–1903

    Article  CAS  Google Scholar 

  • Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG Jr (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424:303–306

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Andrzej, Szymon and Hubert Denis, as well as Józef Liczkowski for collecting the mussels for the experiments. We also deeply acknowledge the help of Arkadiusz Mierzejewski and Krzysztof Puwalski in capturing fish. Our study was supported by a Grant of the Polish Ministry of Science and Higher Education No. NN304 1530 33.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jarosław Kobak.

Additional information

Handling Editor: Piet Spaak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kobak, J., Kakareko, T. The effectiveness of the induced anti-predator behaviour of zebra mussel Dreissena polymorpha in the presence of molluscivorous roach Rutilus rutilus . Aquat Ecol 45, 357–366 (2011). https://doi.org/10.1007/s10452-011-9359-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-011-9359-7

Keywords

Navigation