Chronic contamination decreases disease spread: A daphnia-fungus-copper case study

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1741, 2012, Pages 3146-3153

  Civitello, David J ^a   Forys, Philip ^b   Johnson, Adam P ^a   Hall, Spencer R ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Contamination; Daphnia; Disease; Multi generational effects; Parasite reproduction; Transmission

Indexed keywords

CHEMICAL POLLUTANT; COPPER; CRUSTACEAN; DISEASE SPREAD; DISEASE TRANSMISSION; EPIDEMIC; FUNGUS; HOST-PARASITE INTERACTION; PARAMETERIZATION; PARASITE INTENSITY; SUBLETHAL EFFECT; ZOOPLANKTON;

DAPHNIA; FUNGI;

EID: 84863857847     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0684     Document Type: Article

References (43)

1. Lafferty, K. D., Porter, J. W. & Ford, S. E. 2004 Are diseases increasing in the ocean? Ann. Rev. Ecol. Evol. Syst. 35, 31-54. doi:10.1146/annurev.ecolsys.35.021103.105704
2. Schwarzenbach, R. P., Escher, B. I., Fenner, K., Hofstetter, T. B., Johnson, C. A., von Gunten, U. & Wehrli, B. 2006 The challenge of micropollutants in aquatic systems. Science 313, 1072. doi:10.1126/science.1127291
3. Van Bressem, M.-F. et al. 2009 Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis. Aquat. Organ. 86, 143-157. doi:10.3354/dao02101
4. Khan, R. A. 1990 Parasitism in marine fish after chronic exposure to petroleum hydrocarbons in the laboratory and to the Exxon Valdez oil spill. Bull. Environ. Contam. Toxicol. 44, 759-763. doi:10.1007/BF01701799
5. Rohr, J. R. et al. 2008 Agrochemicals increase trematode infections in a declining amphibian species. Nature 455, 1235-1239. doi:10.1038/nature07281
6. Lafferty, K. D. & Kuris, A. M. 1999 How environmental stress affects the impacts of parasites? Limnol. Oceanogr. 44, 925-931. doi:10.4319/lo.1999.44.3_part_2.0925
7. Lafferty, K. D. & Holt, R. D. 2003 How should environmental stress affect the population dynamics of disease? Ecol. Lett 6, 654-664. doi:10.1046/j.1461-0248.2003.00480.x
8. Chou, H. Y., Peng, T. Y., Chang, S. J., Hsu, Y. L. & Wu, J. L. 1999 Effect of heavy metal stressors and salinity shock on the susceptibility of grouper Epinephelus sp. to infectious pancreatic necrosis virus. Virus Res. 63, 121-129. doi:10.1016/S0168-17029900065-9
9. Griggs, J. & Belden, L. 2008 Effects of Atrazine and metolachlor on the survivorship and infectivity of Echinostoma trivolvis; Trematode Cercariae. Arch. Environ. Contam. Toxicol. 54, 195-202. doi:10.1007/s00244-007-9029-x
10. Rohr, J. R., Raffel, T. R., Sessions, S. K. & Hudson, P. J. 2008 Understanding the net effects of pesticides on amphibian trematode infections. Ecol. Appl. 18, 1743-1753. doi:10.1890/07-1429.1
11. Marshall, D. J. 2008 Transgenerational plasticity in the sea: context-depen dent maternal effects across the life history. Ecology 89, 418-427. doi:10.1890/07-0449.1
12. Ebert, D. 2005 Ecology, epidemiology, and evolutionof parasitism in Daphnia. Bethesda, MD: National Library of Medicine US, National Center for Biotechnology Information.
13. Hall, S. R., Simonis, J. L., Nisbet, R. M., Tessier, A. J. & Caceres, C. E. 2009 Resource ecology of virulence in a planktonic host-parasite system: an explanation using dynamic energy budgets. Am. Nat. 174, 149-162. doi:10.1086/600086
14. van Hullebusch, E., Chatenet, P., Deluchat, V., Chazal, P. M., Froissard, D., Botineau, M., Ghestem, A. & Baudu, M. 2003 Copper accumulation in a reservoir ecosystem following copper sulfate treatment St Germain Les Belles, France. Water, Air Soil Pollut. 150, 3-22. doi:10.1023/A:1026148914108
15. Hutchinson, T. C. & Havas, M. 1986 Recovery of previously acidified lakes near Coniston, Canada following reductions in atmospheric sulphur and metal emissions. Water, Air, Soil Pollut. 28, 319-333. doi:10.1007/BF00583498
16. Bossuyt, B. T. A. & Janssen, C. R. 2004 Influence of multigeneration acclimation to copper on tolerance, energy reserves, and homeostasis of Daphnia magna straus. Environ. Toxicol. Chem. 23, 2029-2037. doi:10.1897/03-377
17. Hall, S. R., Knight, C. J., Becker, C. R., Duffy, M. A., Tessier, A. J. & Caceres, C. E. 2009 Quality matters: resource quality for hosts and the timing of epidemics. Ecol. Lett. 12, 118-128. doi:10.1111/j.1461-0248.2008.01264.x
18. Fernández-González, M. A., González-Barrientos, J., Carter, M.J. & Ramos-Jiliberto, J. 2011 Parent-tooffspring transfer of sublethal effects of copper exposure: metabolic rate and life-history traits of Daphnia. Rev. Chilena Hist. Nat. 84, 195-201. doi:10.4067/S0716-078X2011000200005
19. Anderson, R. M. & May, R. M. 1991 Infectious diseases of humans. Oxford, UK: Oxford University Press.
20. Hall, S. R., Becker, C. R., Duffy, M. A. & Cáceres, C. E. 2010 Variation in resource acquisition and use among host clones creates key epidemiological trade-offs. Am. Nat. 176, 557-565. doi:10.1086/656523
21. Duffy, M. A. & Sivars-Becker, L. 2007 Rapid evolution and ecological host-parasite dynamics. Ecol. Lett. 10, 44-53. doi:10.1111/j.1461-0248.2006.00995.x
22. Carius, H. J., Little, T. J. & Ebert, D. 2001 Genetic variation in host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 1136-1145.
23. Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L. & Ebert, D. 2011 Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype-genotype interactions. Ecol. Lett. 14, 125-131. doi:10.1111/j.1461-0248.2010.01561.x
24. Baer, K. N. & Goulden, C. E. 1998 Evaluation of a highhardness COMBO medium and frozen algae for Daphnia magna. Ecotoxicol. Environ. Saf. 39, 201-206. doi:10.1006/eesa.1997.1627
25. Sarnelle, O. & Wilson, A. E. 2008 Type III functional response in Daphnia. Ecology 89, 1723-1732. doi:10.1890/07-0935.1
26. Hilborn, R. & Mangel, M. 1997 The ecological detective: confronting models with data. Princeton, NJ: Princeton University Press.
27. McCallum, H. 2000 Population parameters: estimation for ecological models. Oxford, UK: Wiley-Blackwell.
28. Sokal, R. R. & Rohlf, F. J. 1995 Biometry, 3rd edn. New York, NY: WH Freeman.
29. Legendre, P. & Legendre, L. 1998 Numerical ecology. Amsterdam, The Netherlands: Elsevier Science.
30. Arneberg, P., Skorping, A., Grenfell, B. & Read, A. F. 1998 Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B 265, 1283-1289. doi:10.1098/rspb.1998.0431
31. Parker, B. J., Elderd, B. D. & Dwyer, G. 2010 Host behaviour and exposure risk in an insect-pathogen interaction. J. Anim. Ecol. 79, 863-870. doi:10.1111/j.1365-2656.2010.01690x
32. Kooijman, S. 2009 Dynamic energy and mass budgets in biological systems. Cambridge, UK: Cambridge University Press.
33. Galloway, T. & Handy, R. 2003 Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12, 345-363. doi:10.1023/A:1022579416322
34. Coors, A. & De Meester, L. 2011 Fitness and virulence of a bacterial endoparasite in an environmentally stressed crustacean host. Parasitology 138, 122-131. doi:10.1017/S0031182010000995
35. Hall, S. R., Becker, C., Duffy, M. A. & Cáceres, C. 2011 Epidemic size determines population-level effects of fungal parasites on Daphnia hosts. Oecologia 166, 833-842. doi:10.1007/s00442-011-1905-4
36. Grindstaff, J. L., Brodie, E. D. & Ketterson, E. D. 2003 Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R. Soc. Lond. B 270, 2309-2319. doi:10.1098/rspb.2003.2485
37. Ben-Ami, F., Ebert, D. & Regroes, R. 2010 Pathogen dose infectivity curves as a method to analyze the distribution of host susceptibility: a quantitative assessment of maternal effects after food stress and pathogen exposure. Am. Nat. 175, 106-115. doi:10.1086/648672
38. Jansen, M., Coors, A., Stoks, R. & De Meester, L. 2011 Evolutionary ecotoxicology of pesticide resistance: a case study. Ecotoxicology 20, 543-551. doi:10.1007/s10646-011-0627-z
39. Jansen, M., Stoks, R., Coors, A., van Doorslaer, W. & De Meester, L. 2011 Collateral damage: rapid exposure-induced evolution of pesticide resistance leads to increased susceptibility to parasites. Evolution 65, 2681-2691. doi:10.1111/j.1558-5646.2011.01331.x
40. Kooi, B. W., Bontje, D., van Voorn, G. A. K. & Kooijman, S. A. L. M. 2008 Sublethal toxic effects in a simple aquatic food chain. Ecol. Model. 212, 304-318. doi:10.1016/j.ecolmodel.2007.10.042
41. Ginzburg, L. R. 1998 Inertial growth: population dynamics based on maternal effects. In Maternal effects as adaptations eds T. Mousseau & C. Fox, pp. 42-53. Oxford, UK: Oxford University Press.
42. Keesing, F., Holt, R. D. & Ostfeld, R. S. 2006 Effects of species diversity on disease risk. Ecol. Lett. 9, 485-498. doi:10.1111/j.1461-0248.2006.00885.x
43. Relyea, R. & Hoverman, J. 2006 Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol. Lett. 9, 1157-1171. doi:10.1111/j.1461-0248.2006.00966.x