Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T19:44:14.591Z Has data issue: false hasContentIssue false
  • English
  • Français

Branchiobdellidan infestation on endangered white-clawed crayfish (Austropotamobius pallipes) in the UK

Published online by Cambridge University Press:  06 February 2012

P. J. ROSEWARNE ,
R. J. G. MORTIMER  and
A. M. DUNN
P. J. ROSEWARNE
Affiliation:
Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
R. J. G. MORTIMER
Affiliation:
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK
A. M. DUNN*
Affiliation:
Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
*
*Corresponding author: Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK. Tel: +44 (0)113 3432856. Fax +44 (0)113 3432835. E-mail: a.dunn@leeds.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Branchiobdellidans or crayfish worms are clitellate annelids and ectosymbionts of freshwater crayfish. An investigation of branchiobdellidan infestation was undertaken in a population of endangered white-clawed crayfish (Austropotamobius pallipes) in the river Aire, UK. Thirty two percent of animals were infested either by the adult parasite or their cocoons (n=107). Parasite burden increased with host size, but did not differ with sex. Observations of crayfish gill tissue revealed a strong positive relationship between melanization of filaments and parasite prevalence and burden. Taxonomic identification revealed that 1 species of branchiobdellidan was present, Branchiobdella astaci. The first sequences were generated for this species and phylogenetically analysed alongside published sequences for 5 other branchiobdellidan species in Europe. The position of B. astaci within the genus Branchiobdella was confirmed, and it was found to cluster as a sister group to B. parasita.

Keywords

Austropotamobius pallipesBranchiobdella astacigill melanizationcrayfish parasite
Type
Research Article
Information
Parasitology , Volume 139 , Issue 6 , May 2012 , pp. 774 - 780
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alberts, A. C., Oliva, M. L., Worley, M. B., Telford, S. R., Morris, P. J. and Janssen, D. L. (1998). The need for pre-release health screening in animal translocations: a case study of the Cuban iguana (Cyclura nubila). Animal Conservation 1, 165–172. doi:10.1111/j.1469-1795.1998.tb00025.x.Google Scholar
Alderman, D. J. and Polglase, J. L. (1988). Pathogens, parasites and commensals. In Freshwater Crayfish Biology Management and Exploitation (eds. Holdich, D. and Lowery, R. S.), pp. 167–212. Timber Press, Portland, Oregon, USA.Google Scholar
Armstrong, D. P. and Seddon, P. J. (2008). Directions in reintroduction biology. Trends in Ecology and Evolution 23, 20–25.CrossRefGoogle ScholarPubMed
Brinkhurst, R. O. (1999). Lumbriculids, branchiobdellidans and leeches: an overview of recent progress in phylogenetic research on clitellates. Hydrobiologia 406, 281–290.CrossRefGoogle Scholar
Brown, B. L., Creed, R. P. and Dobson, W. E. (2002). Branchiobdellid annelids and their crayfish hosts: are they engaged in a cleaning symbiosis? Oecologia 132, 250–255. doi:10.1007/s00442-002-0961-1.CrossRefGoogle Scholar
Cunningham, A. A. (1996). Disease risks of wildlife translocations. Conservation Biology 10, 349–353.CrossRefGoogle Scholar
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161–184.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fureder, L., Summerer, M. and Brandstatter, A. (2009). Phylogeny and species composition of five European species of Branchiobdella (Annelida: Clitellata: Branchiobdellida) reflect the biogeographic history of three endangered crayfish species. Journal of Zoology 279, 164–172. doi:10.1111/j.1469-7998.2009.00601.x.CrossRefGoogle Scholar
Gelder, S. R. (1996). A review of the taxonomic nomenclature and a checklist of the species of the Branchiobdellae (Annelida: Clitellata). Proceedings of the Biological Society of Washington 109, 653–663.Google Scholar
Gelder, S. R. (1999). Zoogeography of branchiobdellidans (Annelida) and temnocephalidans (Platyhelminthes) ectosymbiotic on freshwater crustaceans, and their reactions to one another in vitro. Hydrobiologia 406, 21–31.CrossRefGoogle Scholar
Gelder, S. R. and Brinkhurst, R. O. (1990). An assessment of the phylogeny of the branchiobdellida (annelida, clitellata), using PAUP. Canadian Journal of Zoology-Revue Canadienne De Zoologie 68, 1318–1326.CrossRefGoogle Scholar
Gelder, S. R., Delmastro, G. B. and Ferraguti, M. (1994). A report on branchiobdellidans (annelida, clitellata) and a taxonomic key to the species in northern Italy, including the 1st record of cambarincola-mesochoreus on the introduced American red swamp crayfish. Bollettino Di Zoologia 61, 179–183.CrossRefGoogle Scholar
Gelder, S. R., Delmastro, G. B. and Rayburn, J. N. (1999). Distribution of native and exotic branchiobdellidans (Annelida: Clitellala) on their respective crayfish hosts in northern Italy, with the first record of native Branchiobdella species on an exotic North American crayfish. Journal of Limnology 58, 20–24.CrossRefGoogle Scholar
Gelder, S. R., McCurry, L. and McAlpine, D. F. (2009). Distribution and First Records of Branchiobdellida (Annelida: Clitellata) from Crayfishes (Crustacea: Decapoda) in the Maritime Provinces of Canada. Northeastern Naturalist 16, 45–52.CrossRefGoogle Scholar
Gelder, S. R. and Siddall, M. E. (2001). Phylogenetic assessment of the Branchiobdellidae (Annelida, Clitellata) using 18S rDNA, mitochondrial cytochrome c oxidase subunit I and morphological characters. Zoologica Scripta 30, 215–222.CrossRefGoogle Scholar
Gouin, N., Grandjean, F., Bouchon, D., Reynolds, J. D. and Souty-Grosset, C. (2001). Population genetic structure of the endangered freshwater crayfish Austropotamobius pallipes, assessed using RAPD markers. Heredity 87, 80–87.CrossRefGoogle ScholarPubMed
Grabda, E. and Wierzbicka, J. (1969). The problem of parasitism of the species of the genus Branchiobdella Odier, 1823. Polskie Archiwum Hydrobiologii 16, 93–104.Google Scholar
Holdich, D. M. and Reeve, I. D. (1991). Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquatic Conservation – Marine and Freshwater Ecosystems 1, 139–158.CrossRefGoogle Scholar
Holt, P. (1976). The branchiobdellid (Annelida: Clitellata) associates of astacoidean crawfishes. Freshwater Crayfish 2, 337–346.Google Scholar
Jennings, J. B. and Gelder, S. R. (1979). Gut structure, feeding and digestion in the branchiobdellid oligochaete Cambarincola macrodonta Ellis 1912, an ectosymbiote of the freshwater crayfish Procambarus clarkii. Biological Bulletin 156, 300–314.CrossRefGoogle Scholar
Klobucar, G. I. V., Maguire, I., Gottstein, S. and Gelder, S. R. (2006). Occurrence of Branchiobdellida (Annelida: Clitellata) on freshwater crayfish in Croatia. Annales De Limnologie – International Journal of Limnology 42, 251–260.CrossRefGoogle Scholar
Leeke, C. J. and Price, A. (1965). Branchiobdella astaci in Reading. Reading Naturalist 17, 18–20.Google Scholar
Longshaw, M. (2011). Diseases of crayfish: A review. Journal of Invertebrate Pathology 106, 54–70. doi:10.1016/j.jip.2010.09.013.CrossRefGoogle ScholarPubMed
Mori, M., Pretoni, Y., Salvidio, S. and Balduzzi, A. (2001). Branchiobdellid size-crayfish size: a possible relationship. Journal of Limnology 60, 208–210.CrossRefGoogle Scholar
Oberkofler, B., Quaglio, F., Fureder, L., Fioravanti, M. L., Giannetto, S., Morolli, C. and Minelli, G. (2002). Species of Branchiobdellidae (Annelida) on freshwater crayfish in South Tyrol (Northern Italy). Bulletin Francais De La Peche Et De La Pisciculture 367, 777–784.CrossRefGoogle Scholar
Prenter, J., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385–390. doi: 10.1016/j.tree.2004.05.002.CrossRefGoogle ScholarPubMed
Rogers, D., Hoffmann, R. and Oidtmann, B. (2003). Diseases in selected Austropotamobius pallipes populations in England. In Management and Conservation of Crayfish; Proceedings of a conference held on 7 November 2002 (eds. Holdich, D. and Sibley, P), pp. 169–174. Environment Agency, Bristol.Google Scholar
Schulz, R., Stucki, T. and Souty-Grosset, C. (2002). Management: Reintroductions and restocking. Bulletin Francais De La Peche Et De La Pisciculture 367, 917–922.CrossRefGoogle Scholar
Souty-Grosset, C., Grandjean, F. and Gouin, N. (2003). Involvement of genetics in knowledge, stock management and conservation of Austropotamobius pallipes in Europe. Bulletin Francais De La Peche Et De La Pisciculture 370, 167–179.Google Scholar
Tompkins, D. M., Dunn, A. M., Smith, M. J. and Telfer, S. (2011). Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38. doi: 10.1111/j.1365-2656.2010.01742.x.CrossRefGoogle ScholarPubMed
Van Oosterhout, C., Smith, A. M., Hänfling, B., Ramnarine, I. W., Mohammed, R. S. and Cable, J. (2007). The guppy as a conservation model: implications of parasitism and inbreeding for reintroduction success. Conservation Biology 21, 1573–1583.CrossRefGoogle ScholarPubMed
Viggers, K., Lindenmayer, D. and Spratt, D. (1993). The importance of disease in reintroduction programmes. Wildlife Research 20, 687–698.CrossRefGoogle Scholar
Vogt, G. (1999). Diseases of European freshwater crayfish, with particular emphasis on interspecific transmission of pathogens. In Crayfish in Europe as Alien Species. How to Make the Best of a Bad Situation (eds. Gherardi, F. and Holdich, D.), pp. 87–103. A.A. Balkema, Rotterdam, The Netherlands.Google Scholar
Yue, G. H. and Orban, L. (2005). A simple and affordable method for high-throughput DNA extraction from animal tissues for polymerase chain reaction. Electrophoresis 26, 3081–3083. doi:10.1002/elps.200410411.CrossRefGoogle ScholarPubMed