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Environmental Biology of Fishes

, Volume 97, Issue 5, pp 543–549 | Cite as

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

  • E. Martin Österling
  • Julia Ferm
  • John J. Piccolo
Article

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.

Keywords

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

Notes

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).

References

  1. 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 22:526–532CrossRefGoogle Scholar
  2. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165CrossRefGoogle Scholar
  3. 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 82:817–823CrossRefGoogle Scholar
  4. 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:e36462PubMedCentralPubMedCrossRefGoogle Scholar
  5. 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 29:91CrossRefGoogle Scholar
  6. Fausch K (1984) Profitable stream positions for salmonids - relating specific growth-rate to net energy gain. Can J Zool-Rev Can Zool 62:441–451CrossRefGoogle Scholar
  7. Geist J (2010) Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology. Hydrobiologia 644:69–88CrossRefGoogle Scholar
  8. Gethin R, Taylor J, Garcia de Leaniz C (2013) Does the parasitic freshwater pearl mussel M. margaritifera harm its host? Hydrobiol Early OnlineGoogle Scholar
  9. 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 60:879–886PubMedCrossRefGoogle Scholar
  10. Hastie LC, Young MR (2001) Freshwater pearl mussel (Margaritifera margaritifera) glochidiosis in wild and farmed salmonid stocks in Scotland. Hydrobiologia 445:109–119CrossRefGoogle Scholar
  11. 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 207:171–188CrossRefGoogle Scholar
  12. Hazelton PD, Grossman GD (2009) The effects of turbidity and an invasive species on foraging success of rosyside dace (Cliostomus funduloides). Freshw Biol 54:1977–1988CrossRefGoogle Scholar
  13. Hill J, Grossman G (1993) An energetic model of microhabitat use for rainbow-trout and rosyside dace. Ecology 74:685–698CrossRefGoogle Scholar
  14. 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 47:2039–2048CrossRefGoogle Scholar
  15. 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 60:1462–1476CrossRefGoogle Scholar
  16. 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 12:1–59CrossRefGoogle Scholar
  17. Limm MP, Power ME (2011) Effect of the western pearlshell mussel Margaritifera falcata on Pacific lamprey Lampetra tridentata and ecosystem processes. Oikos 120:1076–1082CrossRefGoogle Scholar
  18. 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 144:2984–2990CrossRefGoogle Scholar
  19. 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 pagesGoogle Scholar
  20. 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 23:564–570CrossRefGoogle Scholar
  21. Österling EM, Greenberg LA, Arvidsson BA (2008) Relationship of biotic and abiotic factors to recruitment patterns in Margaritifera margaritifera. Biol Conserv 141:1365–1370CrossRefGoogle Scholar
  22. 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 47:759–768CrossRefGoogle Scholar
  23. 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 16:432–441CrossRefGoogle Scholar
  24. 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 65:266–275CrossRefGoogle Scholar
  25. Piccolo JJ, Hughes NF, Bryant MD (2008b) Development of net energy intake models for drift-feeding juvenile coho salmon and steelhead. Environ Biol Fish 83:259–267CrossRefGoogle Scholar
  26. 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 acceptedGoogle Scholar
  27. Railsback SF, Harvey BC (2013) Trait-mediated trophic interactions: is foraging theory keeping up? Trends Ecol Evol 28:119–125PubMedCrossRefGoogle Scholar
  28. 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 54:429–439CrossRefGoogle Scholar
  29. 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 58:386–393CrossRefGoogle Scholar
  30. 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 112:1607–1613PubMedCrossRefGoogle Scholar
  31. 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 22:36–46CrossRefGoogle Scholar
  32. Tybout A, Sternthal B (2001) Analysis of variance. J Cons Psych 10:5–35CrossRefGoogle Scholar
  33. Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446CrossRefGoogle Scholar
  34. Vaughn CC, Spooner DE (2006) Unionid mussels influence macroinvertebrate assemblage structure in streams. J N Am Benthol Soc 25:691–700CrossRefGoogle Scholar
  35. Vaughn CC, Gido KB, Spooner DE (2004) Ecosystem processes performed by unionid mussels in stream mesocosms: species roles and effects of abundance. Hydrobiologia 527:35–47CrossRefGoogle Scholar
  36. Young M, Williams J (1983) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland 2. Laboratory studies. Arch Hydrobiol 100:29–43Google Scholar
  37. Young M, Williams J (1984) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland 1. Field studies. Arch Hydrobiol 99:405–422Google Scholar
  38. Zamor RM, Grossman GD (2007) Turbidity affects foraging success of drift-feeding rosyside dace. Trans Am Fish Soc 136:167–176CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • E. Martin Österling
    • 1
  • Julia Ferm
    • 1
  • John J. Piccolo
    • 1
  1. 1.Department of BiologyKarlstad UniversityKarlstadSweden

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