Skip to main content
Log in

Associations between fish reproductive cycle and the dynamics of metazoan parasite infection

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The parasite fauna of the stone loach (Barbatula barbatula) was investigated monthly from May to December 2001. Four parasite species were recorded: Gyrodactylus spp. (Monogenea), Tylodelphys clavata (Digenea), Proteocephalus sagittus (Cestoda), and Raphidascaris acus (Nematoda). The changes in the seasonal dynamics of parasite infection were investigated throughout the 8 months. The potential effect of the reproductive investment of the host, measured by gonad mass and gonado-somatic index (GSI), on the parasite infection was tested against the prediction that, during periods of high reproductive investment (beginning of the breeding period or forming gonads after breeding), the fish are more susceptible to parasite infection. Differences between parasite loads between genders were also hypothesized. Seasonal differences in infection were observed for all parasite species studied. The values of GSI showed a pattern of energy accumulation in the pre-reproductive period and at the beginning of breeding, a decrease during breeding, and an increase in the post-breeding period. A similar pattern was observed for parasite abundance, a strong or weak increase in spring and/or autumn and a decrease during summer (July and August). Positive correlations between the abundance of Gyrodactylus spp. and R. acus and both gonad mass and GSI were found in females after eliminating the effect of fish weight. Our results suggest that stone loach females are more susceptible to parasite infection in periods of higher reproductive investment. The main factor determining the infection of T. clavata was fish size. The abundance of P. sagittus was positively correlated with GSI in the total fish sample with no detectable effect of sex or fish weight. The increase in cestode infection in spring supports the hypothesis that the parasite life cycle could by synchronized with the beginning of host reproduction, probably induced by increasing fish hormone levels in the spring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Baruš V, Oliva O (1995) Petromyzontes and Osteichthyes. Academy of Science of Czech Republic, Prague

  • Buchmann K (1997) Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Dis Aquat Organ 30:145–150

    CAS  Google Scholar 

  • Buchmann K, Moller SH, Uldal A, Bresciani J (1997) Different seasonal infection dynamics of two species of eye-flukes (Displostomum spathaceum and Tylodelphys clavata) in rainbow trout (Oncorhynchus mykiss). Bull Eur Assoc Fish Pathol 17:165–170

    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

    CAS  PubMed  Google Scholar 

  • Chen YF, He DK, Cai B, Chen ZM (2004) The reproductive strategies of an endemic Tibetan fish, Gymnocephalus selincuoensis. J Freshw Ecol 19:255–262

    Google Scholar 

  • Deerenberg C, Apanius V, Daan S, Bos N (1997) Reproductive effort decreases antibody responsiveness. Proc R Soc London B 264:1021–1029

    Article  Google Scholar 

  • Ergens R, Lom J (1970) Causative agents of fish diseases (in Czech). Academia, Prague

  • Georgiev B, Bisekov V, Genov T (1986) The staining method for cestodes with iron acetocarmine. Helminthologia 23:279–281

    Google Scholar 

  • Hanzelová V, Gerdeaux D (2003) Seasonal occurrence of the tapeworm Proteocephalus longicollis and its transmission from copepod intermediate host to fish. Parasitol Res 91:130–136

    Article  PubMed  Google Scholar 

  • Heins DC, Singer SS, Baker JA (1999) Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus. Can J Zool 77:1967–1974

    Article  Google Scholar 

  • Jackson LF, Sullivan CV (1995) Reproduction of white perch—the annual gametogenic cycle. Trans Am Fish Soc 124:563–577

    Article  Google Scholar 

  • Kennedy CR (1981) Long-term studies on the population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata (Digenea: Diplstomatidae), concurrently infecting the eyes of perch, Perca fluviatilis. J Fish Biol 19:221–236

    Google Scholar 

  • Kennedy CR, Burrough R (1977) The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch. J Fish Biol 11:619–633

    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

    Google Scholar 

  • Koskivaara M (1992) Environmental factors affecting monogeneans parasitic on freshwater fishes. Parasitol Today 8:339–342

    Article  CAS  PubMed  Google Scholar 

  • Koskivaara M, Valtonen ET, Prost M (1991) Seasonal occurrence of gyrodactylid monogeneans on the roach (Rutilus rutilus) and variations between four lakes of different water quality in Finland. Aqua Fenn 21:47–55

    Google Scholar 

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

    Article  Google Scholar 

  • McPhail JD, Peacock SD (1983) Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): evolutionary aspects of a host-parasite interaction. Can J Zool 61:901–908

    Google Scholar 

  • Moravec F (2001) Checklist of the metazoan parasites of fish of the Czech Republic and the Slovak Republic. Academia, Prague

  • Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort induces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298

    Article  Google Scholar 

  • Reimchen TE, Nosil P (2001) Ecological causes of sex-biased parasitism in threespine stickleback. Biol J Linn Soc 73:51–63

    Article  Google Scholar 

  • Sanz JJ, Arriero E, Moreno J, Merino S (2001) Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126:339–344

    Article  Google Scholar 

  • Scholz T (1999) Life cycles of species of Proteocephalus, parasites of fishes in the Palearctic region: a review. J Helminthol 73:1–19

    CAS  PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Skarstein F, Folstad I (1996) Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76:359–367

    Google Scholar 

  • Skarstein F, Folstad I, Liljedal S (2001) Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Can J Zool 79:271–278

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  • 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 

  • Valtonen ET, Haaparanta A, Hoffmann RW (1994) Occurrence and histological response of Raphidascaris acus (Nematoda, Ascaridoidea) in roach from four lakes differing in water quality. Int J Parasitol 24:197–206

    Article  CAS  PubMed  Google Scholar 

  • Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174

    Google Scholar 

  • White KAJ, Grenfell BT, Hendry RJ, Lejeune O, Murray JD (1996) Effect of seasonal host reproduction on host-macroparasite dynamics. Math Biosci 137:79–99

    Article  CAS  PubMed  Google Scholar 

  • Zelmer DA, Arai HP (1998) The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. J Parasitol 84:24–28

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the Grant Agency of the Academy of Sciences of the Czech Republic (project no. A 6093104 to M.P., B.K. and V.B.), Grant Agency of the Czech Republic (no. 524/01/1314 to V.B.), Research Project of the Masaryk University (no. MSM 143-1000-10), and Improving Human Potential Programme (COBICE project no. 510). A.Š. was funded by the Grant Agency of the Czech Republic, project no. 524/03/P108. The stay of A.Š. in France was funded by NATO fellowship. We would like to thank Serge Morand and Jean-François Martin from the Centre of Biology and Management of Populations, Montferrier sur Lez, France for useful comments on the first draft. We are very grateful to Iveta Douglas and Carey O. Cunningham from the FRS Marine Laboratory, Aberdeen, Scotland, for correction of the English. The experiments comply with the current laws of our country.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Šimková.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Šimková, A., Jarkovský, J., Koubková, B. et al. Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitol Res 95, 65–72 (2005). https://doi.org/10.1007/s00436-004-1261-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1261-y

Keywords

Navigation