Abstract
In natural host populations, parasitism is considered to be omnipresent and to play an important role in shaping host life history and population dynamics. Here, we study parasitism in natural populations of the zooplankton host Daphnia magna investigating their individual and population level effects during a 2-year field study. Our results revealed a rich and highly prevalent community of parasites, with eight endoparasite species (four microsporidia, one amoeba, two bacteria and one nematode) and six epibionts (belonging to five different taxa: Chlorophyta, Bacillariophyceae, Ciliata, Fungi and Rotifera). Several of the endoparasites were associated with a severe overall fecundity reduction of the hosts, while such effects were not seen for epibionts. In particular, infections by Pasteuria ramosa, White Fat Cell Disease and Flabelliforma magnivora were strongly associated with a reduction in overall D. magna fecundity. Across the sampling period, average population fecundity of D. magna was negatively associated with overall infection intensity and total endoparasite richness. Population density of D. magna was negatively correlated to overall endoparasite prevalence and positively correlated with epibiont richness. Finally, the reduction in host fecundity caused by different parasite species was negatively correlated to both parasite prevalence and the length of the time period during which the parasite persisted in the host population. Consistent with epidemiological models, these results indicate that parasite mediated host damages influence the population dynamics of both hosts and parasites.
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References
Allen YC, DeStasio BT, Ramcharan CW (1993) Individual and population level consequences of an algal epibiont on Daphnia. Limnol Oceanogr 38:592–601
Anderson RM (1982) Population dynamics of infectious diseases: theory and applications. Chapman and Hall, London
Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367
Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, Oxford
Barea-Arco J, Pérez-Martinez C, Morales-Baquero R (2001) Evidence of a mutualistic relationship between an algal epibiont and its host, Daphnia pulicaria. Limnol Oceanogr 46:871–881
Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352
Bengtsson J, Ebert D (1998) Distributions and impacts of microparasites on Daphnia in a rockpool metapopulation. Oecologia 115:213–221
Bittner K, Rothhaupt K-O, Ebert D (2002) Ecological interactions of the microparasite Caullerya mesnili and its host Daphnia galeata. Limnol Oceanogr 47:300–305
Boots M, Sasaki A (2002) Parasite-driven extinction in spatially explicit host-parasite systems. Am Nat 159:706–713
Brambilla DJ (1983) Microsporiodosis in a Daphnia pulex population. Hydrobiologia 99:175–188
Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35
Callan WT, Sanderson SL (2003) Feeding mechanisms in carp: crossflow filtration, palatal protrusions, and flow reversals. J Exp Biol 206:883–892
Carius HJ, Little T, Ebert D (2001) Genetic variation in a host—parasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1146–1152
Chiavelli DA, Mills EL, Threlkeld ST (1993) Host preference, seasonality, and community interactions of zooplankton epibionts. Limnol Oceanogr 38:574–583
Clayton DH, Moore J (1997) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford
De Leo G, Dobson A (2002) Virulence management in Wildlife populations. In: Dieckman U et al (eds) Adaptive dynamics of infectious diseases. In pursuit of virulence management. University Press, Cambridge, pp 413–435
De Meester L, Vandenberghe J, Desender K, Dumont HJ (1994) Genotype-dependent daytime vertical distribution of Daphnia magna in a shallow pond. Belg J Zool 124:3–9
De Meester L, Dawidowicz P, Van Gool E, Loose CJ (1999). Ecology and evolution of predator-induced behaviour of zooplankton: depth selection behaviour and vertical migration. In: Harvell CD, Tollrian R (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 160–176
Decaestecker E, De Meester L, Ebert D (2002) In deep trouble: habitat selection constrained by multiple enemies. Proc Natl Acad Sci USA 99:5481–5485
Decaestecker E, Ebert D, De Meester L (2003) Evidence for strong host clone—parasite species interactions in the Daphnia—microparasite system. Evolution 57:784–792
Decaestecker E, Lefever C, De Meester L, Ebert D (2004) Haunted by the past: evidence for dormant stage banks of Daphnia. Limnol Oceanogr 49:1355–1364
Dobson C, Bowden RJ (1974) Studies on the immunity of sheep to Oesophagostomum columbianum: effects of low-protein diet on resistance to infection and cellular reactions in the gut. Parasitology 69:239–255
Dobson AP, Crawley M (1994) Pathogens and the structure of plant communities. Trends Ecol Evol 9:393–398
Dobson AP, Grenfell BT (1995) Ecology of infectious diseases in natural populations. University Press, Cambridge
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
Ebert D (1995) The ecological interactions between a microsporidian parasite and its host Daphnia magna. J Anim Ecol 64:361–369
Ebert D, Payne RJH, Weisser WW (1997) The epidemiology of parasitic diseases in Daphnia. In: Dettner K, Bauer G, Völkl W (eds) Vrtical food web interactions: evolutionary patterns and driving forces. Springer, Berlin Heidelberg New York, pp 91–111
Ebert D, Zshokke-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 B Biol Sci 265:2127–2134
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
Ebert D, Zschokke-Rohringer CD, Carius HJ (2000b) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122:200–209
Ebert D, Hottinger JW, Pajunen VI (2001) Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82:3417–3434
Ebert D, Carius HJ, Little T, Decaestecker E (2004) The evolution of virulence when parasites cause host castration and gigantism. Am Nat 164:S19-S31
Edmondson WT, Litt AH (1982) Daphnia in lake Washington. Limnol Oceanogr 27:272–293
Fels D, Lee VA, Ebert D (2004) The impact of microparasites on the vertical distribution of Daphnia magna . Arch Hydrobiol 161:65–80
Gandon S, Agnew P, Michalakis Y (2002) Coevolution between parasite virulence and host life-history traits. Am Nat 160:374–388
Green J (1974) Parasites and epibionts of Cladocera. Trans Zool Soc Lond 32:417–515
Gulland FMD (1995) The impact of infectious diseases on wild animal populations-a review. In Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. University Press, Cambridge, pp 20–51
Haag CR, Sakwinska O, Ebert D (2003) Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57:777–783
Hall SR, Duffy MA, Caceres CE (2005) Selective predation and productivity jointly drive complex behavior in host-parasite systems. Am Nat 165:70–81
Hochachka WM, Dhondt AA (2000) Density-dependent decline of host abundance resulting from a new infectious disease. Proc Natl Acad Sci USA 97:5303–5306
Hudson PJ, Dobson AP (1995) Macroparasites: observed patterns in naturally fluctuating animal populations. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 144–176
Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258
Hurd H (2001) Host fecundity reduction: a strategy for damage limitation. Trends Parasitol 17:363–368
Hurst LD (1993) The incidence, mechanisms and evolution of cytoplasmic sex-ratio distorters in animals. Biol Rev 68:121–197
Lafferty KD, Holt RD (2003) How should environmental stress affect the poulation dynamics of disease? Ecol Lett 6:654–664
Mangin KL, Lipsitch M, Ebert D (1995) Virulence and transmission modes of two microsporidia in Daphnia magna. Parasitology 111:133–142
McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystem. Trends Ecol Evol 10:190–194
O’Keefe KJ, Antonovics J (2002) Playing by different rules: the evolution of virulence in sterilizing pathogens. Am Nat 159:597–605
Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herd healthy and alert: implications of predator control for infectious disease. Ecol Lett 6:797–802
Pulkinnen K, Ebert D (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85:823–833
Regoes RR, Hottinger JW, Sygnarski L, Ebert D (2003) The infection rate of D. magna by Pasteuria ramosa conforms with the mass action principle. Epidemiol Infect 131:957–966
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Slater AFG, Keymer AE (1986) Heligmosomoides polygyrus (Nematoda): the influence of dietery protein on the dynamics of repeated infection. Proc R Soc Lond B Biol Sci 229:69–83
Sommer U (1989) Plankton ecology: succession in plankton communities. Springer, Berlin Heidelberg New York
Stirnadel HA, Ebert D (1997) Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. J Anim Ecol 66:212–222
Talling JF, Driver D (1963) Some problems in the estimation of chlorophyll-a in phytoplankton. In: Proceedings of a conference on primary production measurements, marine and freshwater, US Atomic
ter Braak CJF, Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows: software for canonical community ordination (version 4). Microcomputer Power (Ithaca, NY, USA)
Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago
Threlkeld ST, Willey RL (1993) Colonization, interaction, and organization of cladoceran epibiont communities. Limnol Oceanogr 38:584–591
Threlkeld ST, Chiavelli AD, Willey RL (1993) The organization of zooplankton epibiont communities. Trends Ecol Evol 8:317–321
Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parsitol Today 1999:311–313
Tompkins DM., Dobson AP, Arneberg P, Begon ME, Cattadori IM, Greenman JV, Heesterbeek JAP, Hudson PH, Newborn D, Pugliese A, Rizzoli AP, Rosa R, Rosso F, Wilson K (2002). Parasites and host population dynamics. In: Hudson PH et al (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 45–62
Vidtman S (1993) The peculiarities of prevalence of microsporidium Larssonia daphnia in the natural Daphnia pulex population (Russian). Ekologija 1:61–69
Willey RL, Cantrel PA, Threlkeld ST (1990) Epibiotic euglenoid flagellates increase the susceptibility of some zooplankton to fish predation. Limnol Oceanogr 35:952–959
Acknowledgements
We thank Annelies Cappan for practical assistance, Luc Brendonck, Karl Cottenie, Joost Raeymaekers, Robby Stoks, Joost Vanoverbeke and Tom Wenseleers for their comments and discussion on earlier versions of the manuscript. Support for this research was provided by the Flemish Institute of Scientific Research in Industry (IWT), the KULeuven Research Fund (PDM 03/139) and het Fonds voor Wetenschappelijk Onderzoek-Vlaanderen (F.W.O) to ED & SD, by the KULeuven Research Fund (project OT/00/14) to LDM, and by the Swiss Nationalfonds to DE. This field study complies with the current laws of Belgium, in which it was performed.
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Decaestecker, E., Declerck, S., De Meester, L. et al. Ecological implications of parasites in natural Daphnia populations. Oecologia 144, 382–390 (2005). https://doi.org/10.1007/s00442-005-0083-7
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DOI: https://doi.org/10.1007/s00442-005-0083-7