Skip to main content
Springer Nature Link
Log in

Patterns of host switching in the fish ectoparasite Argulus coregoni

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Mating is essential for sexually reproducing species to pass on their genes. For sexual parasites, this implies a need to switch the host in the search for a mate when potential partners are not available on the same host, although host switching includes risks like starvation and predation. Studies of mate-searching behavior predict that commonly only one sex searches for mating partners while the other remains stationary. In the present work, we experimentally infected rainbow trout (Oncorhynchus mykiss) with the fish ectoparasite Argulus coregoni and determined whether the sex, age and the presence of mating partners influenced the host switching activity. Our results show that increased host switching by A. coregoni occurred only after the parasite reached the adult stage and a difference between the sexes was also recorded. Host switching by mature males was enhanced when no mating partners were present on the same host, whereas females remained mainly stationary on their host regardless of male presence or absence. Our data therefore support the hypothesis that there is a strategic difference in reproductive behavior between males and females; males invest energy in mate searching while females are rather stationary and invest into body size and hence increased fecundity. Our data also showed that leaving the host to find a mate is potentially costly in terms of predation since a substantial number of free-swimming parasites were eaten by fish.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Andow DA (1991) Vegetational diversity and arthropod response. Ann Rev Entomol 36:561–586 DOI 10.1146/annurev.en.36.010191.003021

    Article  Google Scholar 

  • Anstensrud M (1989) A vital stain for studies of behavior and ecology of the parasitic copepod Lernaeocera branchialis (Pennellidae). Mar Ecol Prog Ser 53:47–50

    Article  Google Scholar 

  • Bandilla M, Hakalahti T, Hudson PJ, Valtonen ET (2005) Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure? Parasitology 130:169–176 DOI 10.1017/S0031182004006407

    Article  PubMed  CAS  Google Scholar 

  • Bandilla M, Valtonen ET, Suomalainen L-R, Aphalo PJ, Hakalahti T (2006) A link between ectoparasite infection and susceptibility to bacterial disease in rainbow trout. Int J Parasitol 36:987–991 DOI 10.1016/j.ijpara.2006.05.001

    Article  PubMed  CAS  Google Scholar 

  • Brown CR, Brown MB (1996) Coloniality in the cliff swallow. The effect of group size on social behavior. University of Chico Press, Chicago

    Google Scholar 

  • Byers J, Wiseman P, Jones L, Roffe T (2005) A large cost of female mate sampling in pronghorn. Am Nat 166:661–668 DOI 10.1086/497401

    Article  PubMed  Google Scholar 

  • Colorni A (2004) Diseases of Mediterranean fish species: problems, research and prospects. Bull Eur Assoc Fish Pathol 24:22–32

    Google Scholar 

  • Cusack R, Cone DK (1986) A review of parasites as vectors of viral and bacterial diseases of fish. J Fish Dis 9:169–171

    Article  Google Scholar 

  • Dawson LHJ, Renaud JF, Guégan JF, de Meeûs T (2000) Experimental evidence of asymmetrical competition between two species of parasitic copepods. Proc R Soc Lond B 267:1973–1978 DOI 10.1098/rspb.2000.1238

    Article  CAS  Google Scholar 

  • deRivera CE, Vehrencamp SL (2001) Male versus female mate searching in fiddler crabs: a comparative analysis. Behav Ecol 12:182–191

    Article  Google Scholar 

  • deRivera CE, Backwell PRY, Christy JH, Vehrencamp SL (2003) Density affects female and male searching in the fiddler crab, Uca beebei. Behav Ecol Sociobiol 53:72–83 DOI 10.1007/s00265-002-0555-2

    Google Scholar 

  • Fredensborg BL, Poulin R (2005) Larval helminths in intermediate hosts: Does competition early in life determine the fitness of adult parasites? Int J Parasitol 35:1061–1070 DOI 10.1016/j.ijpara.2005.05.005

    Article  PubMed  CAS  Google Scholar 

  • Fretwell SD, Lucas Jr HL (1970) on territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Ghiselin M (1974) The economy of nature and the evolution of sex. University of California Press, Berkeley

    Google Scholar 

  • Gibson RM, Langen TA (1996) How do animals choose their mates? Trends Ecol Evol 11:468–470

    Article  Google Scholar 

  • Gotthard K, Nylin S, Wiklund C (1999) Mating system evolution in response to search costs in the speckled wood butterfly, Pararge aegeria. Behav Ecol Sociobiol 45:424–429 DOI 10.1007/s002650050580

    Article  Google Scholar 

  • Hakalahti T, Valtonen ET (2003) Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitology 127:79–85 DOI 10.1017/S0031182003003196

    Article  PubMed  CAS  Google Scholar 

  • Hakalahti T, Lankinen Y, Valtonen ET (2004a) Efficacy of emamectin benzoate in the control of Argulus coregoni (Crustacea: Branchiura) on rainbow trout Oncorhynchus mykiss. Dis Aquat Org 60:197–204

    Article  PubMed  CAS  Google Scholar 

  • Hakalahti T, Pasternak AF, Valtonen ET (2004b) Seasonal dynamics of egg laying and egg-laying strategy of the ectoparasite Argulus coregoni (Crustacea: Branchiura). Parasitology 128:655–660 DOI 10.1017/S0031182004004986

    Article  PubMed  CAS  Google Scholar 

  • Hakalahti T, Bandilla M, Valtonen ET (2005) Delayed transmission of a parasite is compensated by accelerated growth. Parasitology 131:647–656 DOI 10.1017/S0031182005008279

    Article  PubMed  CAS  Google Scholar 

  • Hakalahti T, Karvonen A, Valtonen ET (2006) Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies. J Helminthol 80:93–98

    Article  PubMed  CAS  Google Scholar 

  • Hammerstein P, Parker GA (1987) Sexual selection: games between the sexes. In: Bradbury JW, Andersson MB (eds) Sexual selection: testing the alternatives. John Wiley & Sons, New York, pp 119–142

    Google Scholar 

  • Hull MQ, Pike AW, Mordue (Luntz) AJ, Rae GH (1998) Patterns of pair formation and mating in an ectoparasitic caligid copepod Lepeoptheirus salmonis (Krøyer 1837): implications for its sensory and mating biology. Phil Trans R Soc Lond B 353:753–764

    Article  Google Scholar 

  • Jaworski A, Holm JC (1992) The distribution and structure of the population of sea lice (Lepeoptheirus salmonis Krøyer) on Atlantic salmon (Salmo salar L.) under typical rearing conditions. Aquacult Fish Mgmt 23:577–589

    Google Scholar 

  • Karvonen A, Paukku S, Seppälä O, Valtonen ET (2005) Resistance against eye flukes: naïve versus previously infected fish. Parasitol Res 95:55–59 DOI 10.1007/s00436-004-1246-x

    Article  PubMed  Google Scholar 

  • Kasumovic MM, Bruce MJ, Herberstein ME, Andrade MCB (2007) Risky mate search and mate preference in the golden orb web-spider (Nephila plumipes). Behav Ecol 18:189–195 DOI 10.1093/beheco/arl072

    Article  Google Scholar 

  • Keeley ER, Grant JWA (1997) Allometry of diet selectivity in juvenile Atlantic salmon (Salmo salar). Can J Fish Aq Sci 54:1894–1902

    Article  Google Scholar 

  • Kollatsch D (1959) Untersuchungen über die Biologie und Ökologie der Karpfenlaus (Argulus foliaceus L.). Zool Beitr 5:1–36

    Google Scholar 

  • Krasnov BR, Burdelova NV, Khokhlova IS, Shenbrot GI, Degen A (2005) Larval interspecific competition in two flea species parasitic on the same rodent host. Ecol Entom 30:146–155 DOI 10.1111/j.0307-6946.2005.00686.x

    Article  Google Scholar 

  • Learmount J, Taylor MA, Smith G, Morgan C (2006) A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms. Vet Parasitol 142:312–329

    Article  PubMed  CAS  Google Scholar 

  • Menezes J, Ramos MA, Pereira TG, da Silva AM (1990) Rainbow trout culture failure in a small lake as a result of massive parasitosis related to careless fish introductions. Aquaculture 89:123–126

    Article  Google Scholar 

  • Mikheev VN, Valtonen ET, Rintamäki-Kinnunen P (1998) Host searching in Argulus foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity. Parasitology 116:425–430

    Article  PubMed  Google Scholar 

  • Mikheev VN, Pasternak AF, Valtonen ET, Lankinen Y (2001) Spatial distribution and hatching of overwintered eggs of a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura). Dis Aquat Org 46:123–128

    Article  PubMed  CAS  Google Scholar 

  • Mikheev VN, Pasternak AF, Valtonen ET (2004) Tuning host specificity during the ontogeny of a fish ectoparasite: behavioral responses to host-induced cues. Parasitol Res 92:220–224 DOI 10.1007/s00436-003-1044-x

    Article  PubMed  Google Scholar 

  • Morris DW (2003) Toward an ecological synthesis: a case of habitat selection. Oecologia 136:1–13 DOI 10.1007/s00442-003-1241-4

    Article  PubMed  Google Scholar 

  • Nishida R, Schulz S, Kim CS, Fukami H, Kuwahara Y, Honda K, Hayashi N (1996) Male sex pheromone of a giant danaine butterfly, Idea leuconoe. J Chem Ecol 22:949–972 DOI 10.1007/BF02029947

    Article  CAS  Google Scholar 

  • Orians GH, Wittenberger JF (1991) Spatial and temporal scales in habitat selection. Am Nat 137:S29–S49

    Article  Google Scholar 

  • Pasternak A, Mikheev V, Valtonen ET (2004) Growth and development of Argulus coregoni (Crustacea: Branchiura) on salmonid and cyprinid hosts. Dis Aquat Org 58:203–207

    Article  PubMed  CAS  Google Scholar 

  • Pirhonen J, Koskela J, Jobling M (1997) Differences in feeding between 1+ and 2 + hatchery brown trout exposed to low water temperature. J Fish Biol 50:678–681 DOI 10.1111/j.1095-8649.1997.tb01960.x

    Article  Google Scholar 

  • Pomiankowski A (1987) The costs of choice in sexual selection. J Theor Biol 128:195–218

    Article  PubMed  CAS  Google Scholar 

  • Proctor HC (1992) Effect of food-deprivation on mate searching and spermatophore production in male water mites (Acari, Unionicolidae). Funct Ecol 53:1987–1994

    Google Scholar 

  • Reynolds J, Gross MR (1990) Costs and benefits of female mate choice: is there a lek paradox? Am Nat 136:230–243

    Article  Google Scholar 

  • Ritchie G (1997) The host transfer ability of Lepeoptheirus salmonis (Copepoda: Caligidae) from farmed Atlantic salmon, Salmo salar L. J Fish Dis 20:153–157 DOI 10.1046/j.1365-2761.1997.00285.x

    Article  Google Scholar 

  • Shimura S (1981) The larval development of Argulus coregoni Thorell (Crustacea: Branchiura). J Nat Hist 15:331–348

    Article  Google Scholar 

  • Shimura S (1983) Seasonal occurrence, sex ratio and site preference of Argulus coregoni Thorell (Crustacea: Branchiura) parasitic on cultured freshwater salmonids in Japan. Parasitology 86:537–552

    Article  Google Scholar 

  • Shirley MA, Hines AH, Wolcott TG (1990) Adaptive significance of habitat selection by molting adult crabs Callinectes sapidus (Rathbun) within a subestuary of central Chesapeake Bay. J Exp Marine Biol Ecol 140:107–119 DOI 10.1016/0022-0981(90)90085-Q

    Article  Google Scholar 

  • Stammer HJ (1959) Beiträge zur Morphologie, Biologie und Bekämpfung der Karpfenläuse. Z Parasitenkd 19:135–208

    Article  CAS  Google Scholar 

  • Tully O, Nolan DT (2002) A review of the population biology and host-parasite interactions of the sea louse Lepeoptheirus salmonis (Copepoda: Caligidae). Parasitology 124:S165–S182 DOI 10.1017/S0031182002001889

    Article  PubMed  Google Scholar 

  • Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled. Cambridge University Press, Cambridge

    Google Scholar 

  • Walker PD, Flik G, Wendelar Bonga SE (2004) The biology of parasites from the genus Argulus and a review of the interactions with its host. In: Wiegertjes GF, Flik G (eds) Host–parasite interactions. Garland Science/BIOS Scientific Publishers, SEB Symposium Series 55, pp 107–129

Download references

Acknowledgement

The authors would like to thank the staff of the Konnevesi research station for support during the experimental work and Prof. Roger Jones for providing valuable comments on the manuscript. Thanks are due to Lenka Trebatická for helpful statistical discussions. This study was financed by the University of Jyväskylä (rector’s grant for M.B.), the Biological Interactions Graduate School of the University of Turku (M.B.), the Ella and Georg Ehrnrooth Foundation (T.H.-S.) and by the Emil Aaltonen Foundation (T.H.-S.). The experiments conducted comply with the current Finnish laws and were approved by the committee for animal welfare of the University of Jyväskylä (22/22.5.2006).

Author information

Authors and Affiliations

  1. Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FIN-40010, University of Jyväskylä, Finland

    Matthias Bandilla, Teija Hakalahti-Sirén & E. Tellervo Valtonen

Authors
  1. Matthias Bandilla
    View author publications

    Search author on:PubMed Google Scholar

  2. Teija Hakalahti-Sirén
    View author publications

    Search author on:PubMed Google Scholar

  3. E. Tellervo Valtonen
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Teija Hakalahti-Sirén.

Additional information

Communicated by P. Heeb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bandilla, M., Hakalahti-Sirén, T. & Valtonen, E.T. Patterns of host switching in the fish ectoparasite Argulus coregoni . Behav Ecol Sociobiol 62, 975–982 (2008). https://doi.org/10.1007/s00265-007-0523-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0523-y

Keywords