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Effects of a Chemically Polluted Discharge on the Relationship Between Fecundity and Parasitic Infections in the Chub (Leuciscus cephalus) from a River in Southern England

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Abstract

In fish there is a close association between endocrine and immune function that during seasonal changes in reproductive status can affect the fishes susceptibility to parasitic infection. The effects of endocrine-disrupting pollution on this association are not known. The present study investigates the effects of a chemically polluted (ammoniacal nitrogen, zinc, bromide) discharge in Cranleigh Waters, a river in southern England, on the fecundity and parasitism of chub, Leuciscus cephalus, over an 18-month period. In the polluted site, the gonado-somatic index (GSI) of fish was lower in females and higher in males compared to an unpolluted upstream site, indicating an androgenic effect on reproduction. Parasite species richness, especially the intestinal helminths Proteocephalus torulosus and Pomphorynchus laevis, was increased in fish in the polluted site. However, the occurrence of the two most common parasite species in the river—Myxobulus sp. 1, a gill myxozoan, and Diplostomum sp., a trematode found in the eye—was unchanged between polluted and unpolluted river sites. Nevertheless, there was a significant relationship between GSI and the prevalence of these two parasite species in the unpolluted site but not the polluted site suggesting that endocrine disruption of reproduction did not lead to an increase in host susceptibility. The reasons for this are discussed.

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References

  • Anonymous (2007) Enquiry into Cranleigh plans. Contam Land Bull (11): 4

  • Boyce NP, Yamada SB (1977) Effects of a parasite, Eubothrium salvelini (Cestoda: Pseudophyllidea), on the resistance of juvenile sockeye salmon, Oncorhynchus nerka, to zinc. J Fish Res Board Can 34:706–709

    CAS  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  Google Scholar 

  • Chubb JC, Pool DW, Veltkamp CJ (1987) A key to the species of cestodes (tapeworms) parasitic in British and Irish freshwater fishes. J Fish Biol 31:517–543

    Article  Google Scholar 

  • Dautremepuits C, Betoulle S, Vernet G (2002) Antioxidant response modulated by copper in healthy or parasitized carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Biochim Biophys Acta 1573:4–8

    CAS  Google Scholar 

  • Dautremepuits C, Betoulle S, Paris-Palacios S, Vernet G (2004) Humoral immune factors modulated by copper and chitosan in healthy or parasitised carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Aquat Toxicol 68:325–338

    Article  CAS  Google Scholar 

  • Dusek L, Gelnar M, Sebelova S (1998) Biodiversity of parasites in a freshwater environment with respect to pollution: metazoan parasites of chub (Leuciscus cephalus L.) as a model for statistical evaluation. Int J Parasitol 28:1555–1571

    Article  CAS  Google Scholar 

  • Fiest SW, Ronga E (1996) Distribution and prevalence of gall blader myxosporean parasites in dab (Limanda limanda L.) and whiting (Merlangius merlangus L.) in UK coastal waters. Bull Eur Assoc Fish Pathol 16:176–180

    Google Scholar 

  • Fisher DJ, Burton DT, Yonkos LT, Turley SD, Ziegler GP (1999) The relative acute toxicity of continuous and intermittent exposures of chlorine and bromine to aquatic organisms in the presence and absence of ammonia. Water Res 33:760–768

    Article  CAS  Google Scholar 

  • Galli P, Crosa G, Mariniello L, Ortis M, D’Amelio S (2001) Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia 452:173–179

    Article  Google Scholar 

  • Hellawell JM (1971) The autecology of the chub, Squalius cephalus (L.), of the River Lugg and the Afon Llynfi. II. Reproduction. Freshw Biol 1:135–148

    Article  Google Scholar 

  • Hoole D (1997) The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39:219–225

    CAS  Google Scholar 

  • Kennedy CR, Hine PM (1969) Population biology of the cestode Proteocephalus torulosus (Batsch) in dace Leuciscus leuciscus (L.) of the River Avon. J Fish Biol 1:209–219

    Article  Google Scholar 

  • Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413

    Article  CAS  Google Scholar 

  • Khan RA, Thulin J (1991) Influence of pollution on parasites of aquatic animals. Adv Parasitol 30:201–238

    Article  CAS  Google Scholar 

  • Kime DE (1998) Endocrine disruption in fish. Kluwer, Boston

    Google Scholar 

  • Kime DE (1999) A strategy for assessing the effects of xenobiotics on fish reproduction. Sci Total Environ 225:3–11

    Article  CAS  Google Scholar 

  • Kime DE, Nash JP (1999) Gamete viability as an indicator of reproductive endocrine disruption in fish. Sci Total Environ 233:123–129

    Article  CAS  Google Scholar 

  • Lamkova K, Simkova A, Palokova M, Jurajda P, Lojek A (2007) Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res 101:775–789

    Article  Google Scholar 

  • Malavasi S, Fiorin R, Franco A, Torricelli P (2004) Somatic energy storage and reproductive investment in the grass goby Zosterisessor ophiocephalus. J Marine Biol Assoc UK 84:455–459

    Article  Google Scholar 

  • Marcogliese DJ, Cone DK (2001) Myxozoan communities parasitizing Notropis hudsonius (Cyprinidae) at selected localities on the St. Lawrence River, Quebec: possible effects of urban effluents. J Parasitol 87:951–956

    CAS  Google Scholar 

  • Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48:197–207

    Article  Google Scholar 

  • Molnár K, Marton Sz, Eszterbauer E, Székely Cs (2006) Comparative morphological and molecular studies on Myxobolus spp. infecting chub from the River Danube, Hungary, and description of M. muellericus sp. n. Dis Aquat Org 73:49–61

    Article  Google Scholar 

  • Morley NJ, Hoole D (1995) Ultrastructural studies on the host-parasite interface between Khawia sinensis (Cestoda: Caryophyllidea) and carp (Cyprinus carpio L.). Dis Aquat Org 23:93–99

    Article  Google Scholar 

  • Morley NJ, Hoole D (1997) The in vitro effect of Khawia sinensis (Cestoda: Caryophyllidea) on leucocyte activity in carp (Cyprinus carpio). J Helminthol 71:47–52

    Article  CAS  Google Scholar 

  • Morley NJ, Crane M, Lewis JW (2002a) Toxicity of cadmium and zinc to cercarial tail loss in Diplostomum spathaceum (Trematoda: Diplostomidae). Parasitology 125:293–301

    Article  CAS  Google Scholar 

  • Morley NJ, Crane M, Lewis JW (2002b) Toxicity of cadmium and zinc mixtures to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. Arch Environ Contam Toxicol 43:28–33

    Article  CAS  Google Scholar 

  • Morley NJ, Crane M, Lewis JW (2003a) Toxicity of cadmium and zinc to the cercarial activity of Diplostomum spathaceum (Trematoda: Diplostomidae). Folia Parasitol 50:57–60

    CAS  Google Scholar 

  • Morley NJ, Irwin SWB, Lewis JW (2003b) Pollutant toxicity to the transmission of larval digeneans through their molluscan intermediate hosts. Parasitology 126:S5–S26

    Article  CAS  Google Scholar 

  • Morley NJ, Lewis JW, Hoole D (2006) Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission. J Helminthol 80:137–149

    Article  CAS  Google Scholar 

  • Nie P, Hoole D (1999) Antibody response of carp Cyprinus carpio to the cestode, Bothriocephalus acheilognathi. Parasitology 118:635–639

    Article  Google Scholar 

  • Orlando EF, Bass DE, Caltabiano LM, Davis WP, Earl Gray L, Guillette LJ Jr (2007) Altered development and reproduction in mosquitofish exposed to pulp and paper mill effluent in the Fenholloway River, Florida USA. Aquat Toxicol 84:399–405

    Article  CAS  Google Scholar 

  • Pietrock M, Marcogliese DJ (2003) Free-living endohelminths: at the mercy of environmental conditions. Trends Parasitol 19:293–299

    Article  Google Scholar 

  • Riggs MR, Esch GW (1987) The suprapopulation dynamics of Bothriocephalus acheilognathi in a North Carolina reservoir: abundance, dispersion, and prevalence. J Parasitol 73:877–892

    Article  CAS  Google Scholar 

  • Schuwerack P-MM, Lewis JW, Hoole D, Morley NJ (2001) Ammonia-induced cellular and immunological changes in juvenile Cyprinus carpio infected with the blood fluke Sanguinicola inermis. Parasitology 122:339–345

    Article  CAS  Google Scholar 

  • Secombes CJ, Chappell LH (1996) Fish immune responses to experimental and natural infection with helminth parasites. Annu Rev Fish Dis 6:167–177

    Article  Google Scholar 

  • Simkova A, Jarkovsky J, Koubkova B, Barus V, Prokes M (2004) Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitol Res 95:65–72

    Article  Google Scholar 

  • Sures B (2006) How parasitism and pollution affect the physiological homeostasis of aquatic hosts. J Helminthol 80:151–157

    Article  CAS  Google Scholar 

  • Suzuki Y, Otaka T, Sato S, Hou YY, Aida K (1997) Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol Biochem 17:415–421

    Article  CAS  Google Scholar 

  • Thames Water (1976–1981) Thames Water statistics, vol 2. Water quality statistics. Thames Water Authority, London

  • Wester PW, Canton JH, Dormans JAMA (1988) Pathological effects in freshwater fish Poecilia reticulata (guppy) and Oryzias latipes (medaka) following methyl bromide and sodium bromide exposure. Aquat Toxicol 12:323–344

    Article  CAS  Google Scholar 

  • Weyts FAA, Cohen N, Flik G, Verburg-Van Kemenade BML (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9:1–20

    Article  Google Scholar 

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Acknowledgments

We would like to thank the staff of Thames Water for their assistance in this study. This article is dedicated to the late Professor Henry Costa, formerly Head of the Department of Zoology, University of Kelaniya, Colombo, Sri Lanka, whose considerable input to the collection of fish data was undertaken during his period of sabbatical leave of absence from Kelaniya spent in the School of Biological Sciences, Royal Holloway, University of London.

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  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    N. J. Morley, H. H. Costa & J. W. Lewis

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  1. N. J. Morley
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  2. H. H. Costa
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  3. J. W. Lewis
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Correspondence to N. J. Morley.

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Morley, N.J., Costa, H.H. & Lewis, J.W. Effects of a Chemically Polluted Discharge on the Relationship Between Fecundity and Parasitic Infections in the Chub (Leuciscus cephalus) from a River in Southern England. Arch Environ Contam Toxicol 58, 783–792 (2010). https://doi.org/10.1007/s00244-009-9386-8

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  • DOI: https://doi.org/10.1007/s00244-009-9386-8

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