Skip to main content
SpringerLink
Log in

Microparasite transmission to Daphnia magna decreases in the presence of conspecifics

  • Population Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Single parasite species often have a range of different hosts which vary in their ability to sustain the parasite. When foraging for food, alternative hosts with similar feeding modes may compete for the infective stages of trophically transmitted parasites. If some of the infective stages end up in unsuitable hosts, transmission of the parasite to the focal host is decreased. I studied whether the presence of conspecifics alters the probability of an uninfected susceptible recipient Daphnia becoming infected by a microparasite and if this effect depends on whether the added conspecifics themselves are susceptible or resistant to infection. The presence of both susceptible and resistant conspecifics decreased the probability of infection in recipients. This effect was dependent on the density of the conspecifics but was not found to be related to their size. In addition, when Daphnia were placed in medium derived from crowded Daphnia populations, the probability of infection in recipients decreased as compared to that in standard medium. This implies that decreases in transmission probability are not caused by dilution of spores through food competition only, but also by indirect interference mediated through infochemicals released by Daphnia. Since Daphnia have been found to respond to crowding by decreasing their filtering rate, the decrease in transmission is probably caused by decreased intake of spores in crowded conditions. The presence of conspecifics can thus decrease microparasite transmission in Daphnia which may have important consequences for epidemiology and evolution of Daphnia parasites.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agnew P, Koella JC (1999) Life-history interactions with environmental conditions in a host–parasite relationship and the parasite’s mode of transmission. Evol Ecol 13:67–89

    Article  Google Scholar 

  • Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc Lond B 291:451–524

    Article  Google Scholar 

  • Anderson RM, May RM (1986) The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos Trans R Soc Lond B 314:533–570

    Article  CAS  Google Scholar 

  • Bittner K, Rothhaupt K-O, Ebert D (2002) Ecological interactions of the microparasite Caullerya mesnili (Chatton 1907) and its host Daphnia galeata from a large lake. Limnol Oceanogr 47:300–305

    Article  Google Scholar 

  • Boersma M, De Meester L, Spaak P (1999) Environmental stress and local adaptation in Daphnia magna. Limnol Oceanogr 44:393–402

    Article  Google Scholar 

  • Burns CW (1969) Relation between filtering rate, temperature, and body size in four species of Daphnia. Limnol Oceanogr 14:693–700

    Article  Google Scholar 

  • Burns CW (1995) Effects of crowding and different food levels on growth and reproductive investment in Daphnia. Oecologia 101:234–244

    Article  PubMed  Google Scholar 

  • Carius H-J, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1136–1145

    Article  CAS  PubMed  Google Scholar 

  • Cleaveland S, et al. (2001) The role of pathogens in biological conservation. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases, 1st edn. Oxford University Press, Oxford, pp 139–150

    Google Scholar 

  • Decaestecker E, Declerck S, De Meester L, Ebert D (2005) Ecological implications of parasites in natural Daphnia populations. Oecologia 144:382–390

    Article  PubMed  Google Scholar 

  • Decaestecker E, Vergote A, Ebert D, De Meester L (2003) Evidence for strong host clone–parasite species interactions in the Daphnia microparasite system. Evolution 57:784–792

    Article  PubMed  Google Scholar 

  • Duffy MA, Hall SR, Tessier AJ, Huebner M (2005) Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control? Limnol Oceanogr 50:412–420

    Article  Google Scholar 

  • Ebert D (1994a) Genetic differences in the interactions of a microsporidian parasite and four clones of its cyclically parthenogenetic host. Parasitology 108:11–16

    Article  Google Scholar 

  • Ebert D (1994b) Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084–1086

    Article  CAS  PubMed  Google Scholar 

  • Ebert D (1995) The ecological interactions between a microsporidian parasite and its host Daphnia magna. J Anim Ecol 64:361–369

    Article  Google Scholar 

  • Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, Md. Available from http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books

  • Ebert D, Lipsitch M, Mangin KL (2000a) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am Nat 156:459–477

    Article  Google Scholar 

  • Ebert D, Mangin KL (1997) The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51:1828–1837

    Article  Google Scholar 

  • Ebert D, Zschokke-Rohringer CD, Carius HJ (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proc R Soc Lond Ser B 265:2127–2134

    Article  Google Scholar 

  • Ebert D, Zschokke-Rohringer CD, Carius HJ (2000b) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122:200–209

    Article  CAS  PubMed  Google Scholar 

  • Fels D (2005) The effect of food on microparasite transmission on the waterflea Daphnia magna. OIKOS 109:360–366

    Article  Google Scholar 

  • Frank S (1996) Models of parasite virulence. Q Rev Biol 71:37–78

    Article  CAS  PubMed  Google Scholar 

  • Franzen C (2004) Microsporidia: how can they invade other cells? Trends Ecol Evol 20:275–279

    CAS  Google Scholar 

  • Gilbert L, Norman R, Laurenson KM, Reid HW, Hudson PJ (2001) Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. J Anim Ecol 70:1053–1061

    Article  Google Scholar 

  • Goser B, Ratte HT (1994) Experimental evidence of negative interference in Daphnia magna. Oecologia 98:354–361

    Article  PubMed  Google Scholar 

  • Haag CR, Ebert D (2004) Parasite-mediated selection in experimental metapopulations of Daphnia magna. Proc R Soc Lond Ser B 271:2149–2155

    Article  Google Scholar 

  • Hayward RS, Gallup DN (1976) Feeding, filtering and assimilations in Daphnia schoedleri SARS as affected by environmental conditions. Arch Hydrobiol 77:139–163

    Google Scholar 

  • Helgen JC (1987) Feeding rate inhibition in crowded Daphnia pulex. Hydrobiologia 154:113–119

    Article  Google Scholar 

  • Holmes JC (1979) Parasite populations and host community stucture. In: Nickol B (ed) Host–parasite interfaces. Academic Press, New York, pp 27–46

    Google Scholar 

  • Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM (2003) Parasite establishment in host communities. Ecol Lett 6:837–842

    Article  Google Scholar 

  • Hosmer DW, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New York

    Book  Google Scholar 

  • Ives AR, Carpenter SR, Dennis B (1999) Community interaction webs and zooplankton responses to planktivory manipulations. Ecology 80:1405–1421

    Article  Google Scholar 

  • Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498

    Article  CAS  PubMed  Google Scholar 

  • Klüttgen B, Dülmer M, Engels M, Ratte HT (1994) ADaM, an artificial freshwater for the culture of zooplankton. Water Res 28:743–746

    Article  Google Scholar 

  • Kopp K, Jokela J (2007) Resistant invaders can convey benefits to native species. Oikos 116:295–301

    Article  Google Scholar 

  • Larsson JI, Ebert D, Vavra J, Voronin VN (1996) Redescription of Pleistophora intestinalis Chatton, 1907, a microsporidian parasite of Daphnia magna and Daphnia pulex, with establishment of the genus Glugoides (Microspora, Glugeidae). Eur J Protistol 32:251–261

    Article  Google Scholar 

  • Little TJ, Ebert D (2000) The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics. Proc R Soc Lond Ser B 267:2037–2042

    Article  CAS  Google Scholar 

  • LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA 100:567–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lürling M, Roozen F, Van Donk E, Goser B (2003) Response of Daphnia to substances released from crowded congeners and conspesifics. J Plankton Res 25:967–978

    Article  Google Scholar 

  • Matveev V (1993) An investigation of allelopathic effects of Daphnia. Freshwater Biol 29:99–105

    Article  Google Scholar 

  • May RM, Anderson RM (1978) Regulation and stability of host-parasite population interactions. II. Destabilizing processes. J Anim Ecol 47:249–267

    Article  Google Scholar 

  • McLean AR, Bostock CJ (2000) Scrapie infections initiated at varying doses: an analysis of 117 titration experiments. Philos Trans R Soc Lond B 355:1043–1050

    Article  CAS  Google Scholar 

  • Murtaugh PA (1985) The influence of food concentration and feeding rate on the gut residence time of Daphnia. J Plankton Res 7:415–420

    Article  Google Scholar 

  • Norman R, Ross D, Laurenson MK, Hudson PJ (2004) The role of non-viraemic transmission on the persistence and dynamics of a tick borne virus—louping ill in red grouse (Lagopus lagopus scoticus) and mountain hares (Lepus timidus). J Math Biol 48:119–134

    Article  PubMed  Google Scholar 

  • Ostfeld RS, Keesing F (2000a) Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 14:722–728

    Article  Google Scholar 

  • Ostfeld RS, Keesing F (2000b) The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 78:2061–2078

    Article  Google Scholar 

  • Pulkkinen K, Ebert D (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85:823–833

    Article  Google Scholar 

  • Pulkkinen K, Ebert D (2006) Persistence of host and parasite populations subject to experimental size-selective removal. Oecologia 149:72–80

    Article  PubMed  Google Scholar 

  • Regoes RR, Ebert D, Bonhoeffer S (2002) Dose-dependent infection rates of parasites produce the Allee effect in epidemiology. Proc R Soc Lond Ser B 269:271–279

    Article  Google Scholar 

  • Regoes RR, Hottinger JW, Sygnarski L, Ebert D (2003) The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiol Infect 131:957–966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt KA, Ostfeld RS (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82:609–619

    Article  Google Scholar 

  • SPSS (2002) SPSS for Windows, release 12.0.1. 2002. SPSS, Chicago, Ill.

  • Tabachnick BG, Fidell LS (2001) Using multivariate statistics, 4th edn. Allyn & Bacon, Boston

    Google Scholar 

  • Telfer S, Brown KJ, Sekule R, Begon M, Hayden T, Birtles R (2005) Distruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130:661–668

    Article  CAS  PubMed  Google Scholar 

  • Valtonen ET, Pulkkinen K, Julkunen M (2003) Getting to the core of the parasite communities: revealing the exchange patterns among sympatric host species. In: Combes C, Jourdane J (eds) Taxonomy, ecology and evolution of metazoan parasites, vol II. PUP, Perpignan, pp 287–303

  • Wolinska J, Keller B, Bittner K, Lass S, Spaak P (2004) Do parasites lower Daphnia hybrid fitness? Limnol Oceanogr 49:1401–1407

    Article  Google Scholar 

Download references

Acknowledgements

Thanks to A. Finne, O. Vuorinen and A. Kleemola for assistance in the laboratory. I also thank T. Marjomäki, P. Aphalo, D. Ebert, S. Lass, S. Aalto and R. Jones for valuable comments on the manuscript and R. Jones for checking the English. Comments from three anonymous referees greatly improved the manuscript. This work was supported by the Academy of Finland.

Author information

Authors and Affiliations

  1. Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, 40014, Jyväskylä, Finland

    Katja Pulkkinen

Authors
  1. Katja Pulkkinen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katja Pulkkinen.

Additional information

Communicated by Ulrich Sommer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pulkkinen, K. Microparasite transmission to Daphnia magna decreases in the presence of conspecifics. Oecologia 154, 45–53 (2007). https://doi.org/10.1007/s00442-007-0805-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0805-0

Keywords

Search

Navigation