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Parasitic freshwater pearl mussel larvae (Margaritifera margaritifera L.) reduce the drift-feeding rate of juvenile brown trout (Salmo trutta L.)

Abstract

In this paper we describe, for the first time, the effects of freshwater pearl mussel (Margaritifera margaritifera L.) encystment on the drift-feeding behavior of juvenile brown trout (Salmo trutta L.). Because both mussel and salmonid populations are often threatened, this study not only adds knowledge to the understanding of host-parasite systems, but it is also of conservation value. Individual trout, mussel-encysted (25.1 ± 5.7 larvae · g−1 body weight, n = 5) or non-encysted (n = 5), were fed with chironomid larvae in a flow-through stream aquarium. Feeding trials were filmed and analyzed by counting the numbers of chironomid larvae each individual ate, and by estimating the prey-capture distance. Non-encysted trout had a significantly higher drift-foraging rate than did encysted trout, and they captured significantly more prey further away from their focal point. The reduced foraging success of encysted trout was mainly due to their failure to catch prey relatively further from their focal point. This suggests that reduced foraging success of encysted trout may be due to poorer energetic status, but the physical effects of mussel larvae on prey handling time cannot be ruled out. Encysted trout caught approximately 20 % fewer prey, which would result in a reduction in growth potential during the period of mussel encystment. Reduced energetic status might also result in reduced competitive ability or in increased exposure to predation risk.

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References

  • Arvidsson BL, Karlsson J, Österling ME (2012) Recruitment of the threatened mussel Margaritifera margaritifera in relation to mussel population size, mussel density and host density. Aquat Conserv Mar Freshwat Ecosyst 22:526–532

    Article  Google Scholar 

  • Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165

    Article  Google Scholar 

  • Crane AL, Fritts AK, Mathis A, Lisek JC, Barnhart MC (2011) Do gill parasites influence the foraging and antipredator behaviour of rainbow darters, Etheostoma caeruleum? Anim Behav 82:817–823

    Article  Google Scholar 

  • Eros T, Gustafsson P, Greenberg LA, Bergman E (2012) Forest-stream linkages: effects of terrestrial invertebrate input and light on diet and growth of brown trout (Salmo trutta) in a boreal forest stream. Plos One 7:e36462

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  • Everest F, Chapman D (1972) Habitat selection and spatial interaction by juvenile Chinook Salmon and Steelhead Trout in 2 Idaho streams. J Fish Res Board Can 29:91

    Article  Google Scholar 

  • Fausch K (1984) Profitable stream positions for salmonids - relating specific growth-rate to net energy gain. Can J Zool-Rev Can Zool 62:441–451

    Article  Google Scholar 

  • Geist J (2010) Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology. Hydrobiologia 644:69–88

    Article  Google Scholar 

  • Gethin R, Taylor J, Garcia de Leaniz C (2013) Does the parasitic freshwater pearl mussel M. margaritifera harm its host? Hydrobiol Early Online

  • Haag WR, Warren ML (2000) Effects of light and presence of fish on lure display and larval release behaviours in two species of freshwater mussels. Anim Behav 60:879–886

    PubMed  Article  Google Scholar 

  • Hastie LC, Young MR (2001) Freshwater pearl mussel (Margaritifera margaritifera) glochidiosis in wild and farmed salmonid stocks in Scotland. Hydrobiologia 445:109–119

    Article  Google Scholar 

  • Hayes JW, Hughes NF, Kelly LH (2007) Process-based modelling of invertebrate drift transport, net energy intake and reach carrying capacity for drift-feeding salmonids. Ecol Model 207:171–188

    Article  Google Scholar 

  • Hazelton PD, Grossman GD (2009) The effects of turbidity and an invasive species on foraging success of rosyside dace (Cliostomus funduloides). Freshw Biol 54:1977–1988

    Article  Google Scholar 

  • Hill J, Grossman G (1993) An energetic model of microhabitat use for rainbow-trout and rosyside dace. Ecology 74:685–698

    Article  Google Scholar 

  • Hughes N, Dill L (1990) Position choice by drift-feeding salmonids - model and test for arctic grayling (Thymallus arcticus) in sub-arctic mountain streams, Interior Alaska. Can J Fish Aquat Sci 47:2039–2048

    Article  Google Scholar 

  • Hughes N, Hayes J, Shearer K, Young R (2003) Testing a model of drift-feeding using three-dimensional videography of wild brown trout, Salmo trutta, in a New Zealand river. Can J Fish Aquat Sci 60:1462–1476

    Article  Google Scholar 

  • Klemetsen A, Amundsen PA, Dempson JB, Jonsson B, Jonsson N, O’Connell MF, Mortensen E (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecol Freshw Fish 12:1–59

    Article  Google Scholar 

  • Limm MP, Power ME (2011) Effect of the western pearlshell mussel Margaritifera falcata on Pacific lamprey Lampetra tridentata and ecosystem processes. Oikos 120:1076–1082

    Article  Google Scholar 

  • Österling EM (2011) Test and application of a non-destructive photo-method investigating the parasitic stage of the threatened mussel Margaritifera margaritifera on its host fish Salmo trutta. Biol Conserv 144:2984–2990

    Article  Google Scholar 

  • Österling EM, Högberg JO (2013) The impact of land use on the mussel Margaritifera margaritifera and its host fish Salmo trutta. Hydrobiol Early Online. doi:10.1007/s10750-013-1501-1, 8 pages

    Google Scholar 

  • Österling ME, Larsen BM (2013) Impact of origin and condition of host fish (Salmo trutta) on parasitic larvae of Margaritifera margaritifera. Aquat Conserv Mar Freshwat Ecosyst 23:564–570

    Article  Google Scholar 

  • Österling EM, Greenberg LA, Arvidsson BA (2008) Relationship of biotic and abiotic factors to recruitment patterns in Margaritifera margaritifera. Biol Conserv 141:1365–1370

    Article  Google Scholar 

  • Osterling ME, Arvidsson BL, Greenberg LA (2010) Habitat degradation and the decline of the threatened mussel Margaritifera margaritifera: influence of turbidity and sedimentation on the mussel and its host. J Appl Ecol 47:759–768

    Article  Google Scholar 

  • Piccolo JJ, Hughes NF, Bryant MD (2007) The effects of water depth on prey detection and capture by juvenile coho salmon and steelhead. Ecol Freshw Fish 16:432–441

    Article  Google Scholar 

  • Piccolo JJ, Hughes NF, Bryant MD (2008a) Water velocity influences prey detection and capture by drift-feeding juvenile coho salmon (Oncorhynchus kisutch) and steelhead (Oncorhynchus mykiss irideus). Can J Fish Aquat Sci 65:266–275

    Article  Google Scholar 

  • Piccolo JJ, Hughes NF, Bryant MD (2008b) Development of net energy intake models for drift-feeding juvenile coho salmon and steelhead. Environ Biol Fish 83:259–267

    Article  Google Scholar 

  • Piccolo JJ, Frank B, Hayes JW (2014) Food and space revisited: The role of drift-feeding theory in predicting the distribution, growth, and abundance of stream salmonids. Environ Biol Fish accepted

  • Railsback SF, Harvey BC (2013) Trait-mediated trophic interactions: is foraging theory keeping up? Trends Ecol Evol 28:119–125

    PubMed  Article  Google Scholar 

  • Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, Nichols SJ (2004) Changing perspectives on pearly mussels, North America’s most imperiled animals. Bioscience 54:429–439

    Article  Google Scholar 

  • Sweka J, Hartman K (2001) Effects of turbidity on prey consumption and growth in brook trout and implications for bioenergetics modeling. Can J Fish Aquat Sci 58:386–393

    Article  Google Scholar 

  • Taeubert J, Geist J (2013) Critical swimming speed of brown trout (Salmo trutta) infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia and implications for artificial breeding of an endangered mussel species. Parasitol Res 112:1607–1613

    PubMed  Article  Google Scholar 

  • Taeubert J, Gum B, Geist J (2012) Host-specificity of the endangered thick-shelled river mussel (Unio crassus, Philipsson 1788) and implications for conservation. Aquat Conserv-Mar Freshw Ecosyst 22:36–46

    Article  Google Scholar 

  • Tybout A, Sternthal B (2001) Analysis of variance. J Cons Psych 10:5–35

    Article  Google Scholar 

  • Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446

    Article  Google Scholar 

  • Vaughn CC, Spooner DE (2006) Unionid mussels influence macroinvertebrate assemblage structure in streams. J N Am Benthol Soc 25:691–700

    Article  Google Scholar 

  • Vaughn CC, Gido KB, Spooner DE (2004) Ecosystem processes performed by unionid mussels in stream mesocosms: species roles and effects of abundance. Hydrobiologia 527:35–47

    Article  Google Scholar 

  • Young M, Williams J (1983) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland 2. Laboratory studies. Arch Hydrobiol 100:29–43

    Google Scholar 

  • Young M, Williams J (1984) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland 1. Field studies. Arch Hydrobiol 99:405–422

    Google Scholar 

  • Zamor RM, Grossman GD (2007) Turbidity affects foraging success of drift-feeding rosyside dace. Trans Am Fish Soc 136:167–176

    Article  Google Scholar 

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Acknowledgments

We thank Fortums nordiska miljöfond, the Knowledge Foundation and Karlstad University for financing this study, and the land owners, fishing organizations and the County Administration Board in Västernorrland for permissions. The study was approved by the Board of Agriculture (Dnr A 54-10).

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Correspondence to E. Martin Österling.

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Österling, E.M., Ferm, J. & Piccolo, J.J. Parasitic freshwater pearl mussel larvae (Margaritifera margaritifera L.) reduce the drift-feeding rate of juvenile brown trout (Salmo trutta L.). Environ Biol Fish 97, 543–549 (2014). https://doi.org/10.1007/s10641-014-0251-x

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  • DOI: https://doi.org/10.1007/s10641-014-0251-x

Keywords

  • Host
  • Parasite
  • Unionid mussels
  • Margaritifera
  • Salmo trutta
  • Drift-feeding
  • Foraging
  • Conservation