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Infection with cerebral metacercariae of microphallid trematode parasites reduces reproductive output in the gammarid amphipod Gammarus insensibilis (Stock 1966) in UK saline lagoons

Published online by Cambridge University Press:  09 May 2017

Andrew R. Gates ,
Martin Sheader ,
John A. Williams  and
Lawrence E. Hawkins
Andrew R. Gates*
Affiliation:
National Oceanography Centre, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK Ocean and Earth Science, National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK
Martin Sheader
Affiliation:
Ocean and Earth Science, National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK
John A. Williams
Affiliation:
Ocean and Earth Science, National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK
Lawrence E. Hawkins
Affiliation:
Ocean and Earth Science, National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK
*
Correspondence should be addressed to: A.R. Gates, National Oceanography Centre, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK email: arg3@noc.ac.uk
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Abstract

Saline lagoons are priority habitats in the United Kingdom supporting several protected specialist species. One specialist, the amphipod Gammarus insensibilis, is infected with behaviour-altering microphallid trematodes such as Microphallus papillorobustus. In saline lagoons around the coast of England (Gilkicker and Lymington–Keyhaven on the Hampshire coast and Moulton Marsh in Lincolnshire) there is variation in the prevalence of this parasite in the gammarid populations (0 at Salterns in the Lymington–Keyhaven lagoon system to 98% at Gilkicker). Infection intensity ranged from 0 to 20 metacercariae in individual amphipods. Higher infection intensity can alter the shape of the amphipod's head. Under experimental conditions respiration rate is significantly reduced in infected animals and reproductive output (expressed as early stage embryos mg g dry weight−1) is significantly lower in infected females. It is important to consider the role of host–parasite interactions in order to understand the ecology of specialist lagoon species such as G. insensibilis and their lagoon habitats.

Keywords

Behaviour modificationmanipulative parasitereproductive investmentChaetomorpha linumMicrophallus papillorobustus
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 6 , September 2018 , pp. 1391 - 1400
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Al-Suwailem, A.M. (1991) The ecology of a saline lagoon in southern England. PhD thesis, University of Southampton, Southampton.Google Scholar
Arnal, A., Droit, A., Elguero, E., Ducasse, H., Sánchez, M.I., Lefevre, T., Misse, D., Bédèrina, M., Vittecoq, M., Daoust, S. and Thomas, F. (2015) Activity level and aggregation behaviour in the crustacean gammarid Gammarus insensibilis parasitized by the manipulative trematode Microphallus papillorobustus. Frontiers in Ecology and Evolution 3, 109.Google Scholar
Bamber, R.N., Batten, S.D., Sheader, M. and Bridgewater, N.D. (1992) On the ecology of brackish water lagoons in Great Britain. Aquatic Conservation: Marine and Freshwater Systems 2, 65–94.Google Scholar
Bamber, R.N., Gilliland, P.M. and Shardlow, E.A. (2001) Saline lagoons: a guide to their management and creation. Saline Lagoon Working Group. Peterborough: English Nature, 95 pp.Google Scholar
Barnes, R.S.K. (1980) Coastal Lagoons: the natural history of a neglected habitat. Cambridge: Cambridge University Press.Google Scholar
Barnes, R.S.K. (1991) Dilemmas in the theory and practice of biological conservation as exemplified by British coastal lagoons. Biological Conservation 55, 315–328.Google Scholar
Beer, N.A. and Joyce, C.B. (2013) North Atlantic coastal lagoons: conservation, management and research challenges in the twenty-first century. Hydrobiologia 701, 1–11.Google Scholar
Brown, S.P., De Lorgeril, J., Joly, C. and Thomas, F. (2003) Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668–672.Google Scholar
Costa, F.O., Cunha, M.R., Neuparth, T., Theodorakis, C.W., Costa, M.H. and Shugart, L.R. (2004) Application of RAPD DNA fingerprinting in taxonomic identification of amphipods: a case-study with Gammarus species (Crustacea: Amphipoda). Journal of the Marine Biological Association of the United Kingdom 84, 171–178.Google Scholar
Dorgelo, J. (1977) Comparative ecophysiology of gammarids (Crustacea: Amphipoda) from marine, brackish and fresh-water habitats exposed to the influence of salinity-temperature combinations. III. Oxygen uptake. Netherlands Journal of Sea Research 7, 253–266.Google Scholar
Ford, A.T., Fernandes, T.F., Rider, S.A., Read, P.A., Robinson, C.D. and Davies, I.M. (2003) Measuring sublethal impacts of pollution on reproductive output of marine Crustacea. Marine Ecology – Progress Series 265, 303–309.Google Scholar
Fredensborg, B.L., Mouritsen, K.N. and Poulin, R. (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.Google Scholar
Garnacho, E., Peck, L.S. and Tyler, P.A. (2001) Effects of copper exposure on the metabolism of the mysid Praunus flexuosus. Journal of Experimental Marine Biology and Ecology 265, 181–201.Google Scholar
Gates, A.R. (2006) The physiological ecology of the specialist lagoon amphipod, Gammarus insensibilis. PhD thesis, University of Southampton, Southampton.Google Scholar
Gilliland, P.M. and Sanderson, W.G. (2000) Re-evaluation of marine benthic species of nature conservation importance: a new perspective on certain ‘lagoonal specialists’ with particular emphasis on Alkmaria romijni Horst (Polychaeta: Ampharetidae). Aquatic Conservation: Marine and Freshwater Ecosystems 10, 1–12.Google Scholar
Guler, Y., Short, S., Etxabe, A.G., Sherhod, C.M., Kille, P. and Ford, A.T. (2015) Impacts of a newly identified behaviour-altering trematode on its host amphipod: from the level of gene expression to population. Parasitology 142, 1469–1480.Google Scholar
Helluy, S. (1983) Relations hôtes-parasites du trématode Microphallus papillorobustus (Rankin 1940). II. Modifications du comportement des Gammarus hôtes intermediaires et localisation des métacercaires. Annales de Parasitologie Humaine et Comparee 58, 1–17.Google Scholar
Helluy, S. (1984) Relations hotes-parasites du trematode Microphallus papillorobustus (Rankin, 1940). III Facteurs impliques dans les modifications du comporttement des Gammarus hotes intermediaires et tests de predation. Annales de Parasitologie Humaine et Comparee 59, 41–56.Google Scholar
Helluy, S. and Holmes, J.C. (1990) Serotonin, octopamine and the clinging behaviour induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Canadian Journal of Zoology 68, 1214–1220.Google Scholar
Helluy, S. and Thomas, F. (2003) Effects of Microphallus papillorobustus (Platyhelminthes : Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proceedings of the Royal Society of London Series B – Biological Sciences 270, 563–568.Google Scholar
Hill, D., Rushton, S.P., Clark, N., Green, P. and Prysjones, R. (1993) Shorebird communities on British estuaries – factors affecting community composition. Journal of Applied Ecology 30, 220–234.Google Scholar
Jensen, K.T., Ferreira, S.M. and Pardal, M.A. (2004) Trematodes in a Cyathura carinata population from a temperate intertidal estuary: infection patterns and impact on host. Journal of the Marine Biological Association of the United Kingdom 84, 1151–1158.Google Scholar
Johnson, W.S., Stevens, M. and Watling, L. (2001) Reproduction and development of marine peracaridans. In Southward, A.J., Tyler, P.A., Young, C.M. and Fuiman, L.A. (eds) Advances in marine biology, Volume 39. London: Academic Press, pp. 105–260.Google Scholar
Karakiri, M. and Nicolaidou, A. (1987) Population studies on the Amphipoda of Mazoma Lagoon (Greece). Helgolander Meeresuntersuchungen 41, 453–464.Google Scholar
Kolding, S. and Fenchel, T.M. (1981) Patterns of reproduction in different populations of five species of the amphipod genus Gammarus. Oikos 37, 167–172.Google Scholar
Kostadinova, A. and Mavrodieva, A.S. (2005a) Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: manipulation hypothesis going east? Parasitology 131, 337–346.Google Scholar
Kostadinova, A. and Mavrodieva, R.S. (2005b) Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: host response to infection. Parasitology 131, 347–354.Google Scholar
Lafferty, K.D. (1996) Altered behaviour of parasitized killifish increased susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.Google Scholar
Maynard, B.J., DeMartini, L. and Wright, W.G. (1996) Gammarus lacustris harboring Polymorphus paradoxus show altered patterns of serotonin-like immunoreactivity. Journal of Parasitology 82, 663–666.Google Scholar
Mouritsen, K.N. and Jensen, K.T. (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123–134.Google Scholar
Mouritsen, K.N. and Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.Google Scholar
Nelson, W.G. (1980) Reproductive patterns of gammaridean amphipods. Sarsia 65, 61–71.Google Scholar
Ottaviani, E. and Franceschi, C. (1996) The neuroimmunology of stress from invertebrates to man. Progress in Neurobiology 48, 421–440.Google Scholar
Pearson, C.V.M., Rogers, A.D. and Sheader, M. (2002) The genetic structure of the rare lagoonal sea anemone, Nematostella vectensis Stephenson (Cnidaria; Anthozoa) in the United Kingdom based on RAPD analysis. Molecular Ecology 11, 2285–2293.Google Scholar
Ponton, F., Biron, D.G., Joly, C., Helluy, S., Duneau, D. and Thomas, F. (2005) Ecology of parasitically modified populations: a case study from a gammarid-trematode system. Marine Ecology Progress Series 299, 205–215.Google Scholar
Rebecq, J. (1964) Recherches Systématiques, Biologiques et Écologiques sur les Formes Larvaires de Quelques Trématodes de Camargue. PhD thesis, University of Marseille, Marseille.Google Scholar
Rumpus, A.E. and Kennedy, C.R. (1974) The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology 68, 271–284.Google Scholar
Saintemarie, B. (1991) A review of the reproductive bionomics of aquatic gammaridean amphipods – variation of life-history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223, 189–227.Google Scholar
Schwartz, S.S. and Cameron, G.N. (1993) How do parasites cost their hosts? Preliminary answers from trematodes and Daphnia obtusa. Limnology and Oceanography 38, 602–612.Google Scholar
Sheader, M. (1996) Factors influencing egg size in the gammarid amphipod Gammarus insensibilis. Marine Biology 124, 519–526.Google Scholar
Sheader, M. and Chia, F.-S. (1970) Development, fecundity and brooding behaviour of the amphipod, Marinogammarus obtusatus. Journal of the Marine Biological Association of the United Kingdom 50, 1079–1099.Google Scholar
Sheader, M. and Sheader, A.L. (1985) New distribution records for Gammarus insensibilis Stock, 1966, in Britain. Crustaceana 49, 101–105.Google Scholar
Sheader, M. and Sheader, A.L. (1987) The distribution of the lagoonal amphipod Gammarus insensibilis stock in England. Porcupine Newsletter 3, 220–223.Google Scholar
Steele, D.H. and Steele, V.J. (1975) The biology of Gammarus (Crustacea, Amphipoda) in the northwestern Atlantic. XI. Comparison and discussion. Canadian Journal of Zoology 53, 1116–1126.Google Scholar
Tain, L., Perrot-Minnot, M.-J. and Cézilly, F. (2007) Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species. Biology Letters 3, 69–72.Google Scholar
The Council of the European Communities (1992) Council directive 92/43/EEC of 21 May 1992 on conservation of natural habitats and of wild fauna and flora, pp. 7–50.Google Scholar
Thomas, F., Adamo, S. and Moore, J. (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.Google Scholar
Thomas, F., Crivelli, A., Cezilly, F., Renaud, F. and deMeeus, T. (1997) Parasitism and ecology of wetlands: a review. Estuaries 20, 646–654.Google Scholar
Thomas, F. and Renaud, F. (2001) Microphallus papillorobustus (Trematoda): a review of its effects in lagoon ecosystems. Revue d'Ecologie – La Terre et la Vie 56, 147–156.Google Scholar
Thomas, F., Renaud, F. and Cezilly, F. (1996a) Assortative pairing by parasitic prevalence in Gammarus insensibilis (Amphipoda): patterns and processes. Animal Behaviour 52, 683–690.Google Scholar
Thomas, F., Renaud, F., de Meeus, T. and Poulin, R. (1998a) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London Series B-Biological Sciences 265, 1091–1096.Google Scholar
Thomas, F., Renaud, F., Derothe, J.M., Lambert, A., Meeüs, T. and Cézilly, F. (1995) Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite. Oecologia 104, 259–264.Google Scholar
Thomas, F., Verneau, O., Santalla, F., Cezilly, F. and Renaud, F. (1996b) The influence of intensity of infection by a trematode parasite on the reproductive biology of Gammarus insensibilis (Amphipoda). International Journal for Parasitology 26, 1205–1209.Google Scholar
Thomas, F., Villa, M., Montoliu, I., Santalla, F., Cezilly, F. and Renaud, F. (1998b) Analyses of a debilitating parasite (Microphallus papillorobustus, Trematoda) and its ‘hitchhiker’ parasite (Maritrema subdolum, Trematoda) on survival of their intermediate host (Gammarus insensibilis, Amphipoda). Journal of the Helminthological Society of Washington 65, 1–5.Google Scholar