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Effect of copper contamination on zooplankton epidemics. (English) Zbl 1411.92265
Summary: Infectious disease and chemical contamination are increasingly becoming vital issues in many ecosystems. However, studies integrating the two are surprisingly rare. Contamination not only affects the inherent host-resource interaction which influences the epidemic process but may also directly affect epidemiological traits via changes in host’s behaviour. The fact that heavy metal such as copper is also an essential trace element for organisms, further increase complexity which make predicting the resultant effect of contamination and disease spread difficult. Motivated by this, we model the effect of copper enrichment on a phytoplankton-zooplankton-fungus system. We show that extremely deficient or toxic copper may have a destabilizing effect on the underlying host-resource dynamics due to increased relative energy fluxes as a result of low host mortality due to fish predation. Further, on incorporating disease into the system, we find that the system can become disease-free for an intermediate range of copper concentration whereas it may persist for very less copper enrichment. Also, we predict that there may exist vulnerable regions of copper concentration near the toxic and deficient levels, where the parasite can invade the system for a comparatively lower spore yield. Overall, our results demonstrate that, the effect of contamination may be fundamental to understanding disease progression in community ecology.
92D30 Epidemiology
92D40 Ecology
Full Text: DOI
[1] Anderson, R. M.; May, R. M., The invasion, persistence and spread of infectious diseases within animal and plant communities, Phil. Trans. R. Soc. Lond. B, 314, 1167, 533-570, (1986)
[2] Armstrong, R. A.; McGehee, R., Competitive exclusion, Am. Nat., 115, 151-170, (1980)
[3] Bossuyt, B. T.; Janssen, C. R., Acclimation of Daphnia magna to environmentally realistic copper concentrations, Comp. Biochem. Physiol. C Toxicol. Pharmacol., 136, 253-264, (2003)
[4] Cáceres, C.; Davis, G.; Duple, S.; Hall, S.; Koss, A.; Lee, P.; Rapti, Z., Complex Daphnia interactions with parasites and competitors, Math. Biosci., 258, 148-161, (2014) · Zbl 1314.92122
[5] Cáceres, C. E.; Tessier, A. J.; Duffy, M. A.; Hall, S. R., Disease in freshwater zooplankton: what have we learned and where are we going?, J. Plankton. Res., 36, 2, 326-333, (2014)
[6] Camara, B. I.; Yamapi, R.; Mokrani, H., How do copper contamination pulses shape the regime shifts of phytoplankton-zooplankton dynamics?, Commun. Nonlinear Sci. Numer. Simul., 48, 170-178, (2017)
[7] Civitello, D. J.; Forys, P.; Johnson, A. P.; Hall, S. R., Chronic contamination decreases disease spread: a Daphnia-fungus-copper case study, Proc. R. Soc. Lond. B Biol. Sci., 279, 3146-3153, (2012)
[8] Clements, W. H.; Cherry, D. S.; Hassel, J. H.V., Assessment of the impact of heavy metals on benthic communities at the Clinch River (Virginia): evaluation of an index of community sensitivity, Can. J. Fish Aquat. Sci., 49, 1686-1694, (1992)
[9] Coors, A.; Decaestecker, E.; Jansen, M.; De Meester, L., Pesticide exposure strongly enhances parasite virulence in an invertebrate host model, Oikos, 117, 12, 1840-1846, (2008)
[10] Cuco, A. P.; Abrantes, N.; Gonçalves, F.; Wolinska, J.; Castro, B. B., Interplay between fungicides and parasites: Tebuconazole, but not copper, suppresses infection in a Daphnia-Metschnikowia experimental model, PLoS ONE, 12, 1-16, (2017)
[11] De Castro, F.; Bolker, B., Mechanisms of disease-induced extinction, Ecol. Lett., 8, 117-126, (2005)
[12] Dhooge, A.; Govaerts, W.; Kuznetsov, Y. A.; Meijer, H. G.E.; Sautois, B., New features of the software matcont for bifurcation analysis of dynamical systems, Math. Comput. Model Dyn. Syst., 14, 2, 147-175, (2008) · Zbl 1158.34302
[13] Diekmann, O.; Heesterbeek, J.; Roberts, M., The construction of next-generation matrices for compartmental epidemic models, J. R. Soc. Interface, 7, 873-885, (2010)
[14] Fargašová, A.; Bumbálová, A.; Havránek, E., Ecotoxicological effects and uptake of metals \(C u^+, C u^{2 +}, M n^{2 +}, M o^{6 +}, N i^{2 +}, V^{5 +}\) in freshwater alga Scenedesmus quadricauda, Chemosphere, 38, 1165-1173, (1999)
[15] Fenton, A.; Rands, S., The impact of parasite manipulation and predator foraging behavior on predator-prey communities, Ecology, 87, 2832-2841, (2006)
[16] Gerritsen, J.; Strickler, J. R., Encounter probabilities and community structure in zooplankton: a mathematical model, J. Fish Res. Board Can., 34, 1, 73-82, (1977)
[17] Gutierrez, M. F.; Paggi, J. C.; Gagneten, A. M., Microcrustaceans escape behavior as an early bioindicator of copper, chromium and endosulfan toxicity, Ecotoxicology, 21, 428-438, (2012)
[18] Hall, S. R.; Becker, C. R.; Duffy, M. A.; Cáceres, C. E., Variation in resource acquisition and use among host clones creates key epidemiological trade-offs, Am. Nat., 176, 557-565, (2010)
[19] Hall, S. R.; Knight, C. J.; Becker, C. R.; Duffy, M. A.; Tessier, A. J.; Cáceres, C. E., Quality matters: resource quality for hosts and the timing of epidemics, Ecol. Lett., 12, 118-128, (2009)
[20] Hall, S. R.; Simonis, J. L.; Nisbet, R. M.; Tessier, A. J.; Cáceres, C. E., Resource ecology of virulence in a planktonic host-parasite system: an explanation using dynamic energy budgets, Am. Nat., 174, 149-162, (2009)
[21] Hall, S. R.; Tessier, A. J.; Duffy, M. A.; Huebner, M.; Cáceres, C. E., Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics, Ecology, 87, 7, 1684-1695, (2006)
[22] Haque, M.; Venturino, E., An eco-epidemiological model with disease in predator: the ratio-dependent case, Math. Methods Appl. Sci., 30, 1791-1809, (2007) · Zbl 1126.92050
[23] Havens, K. E., Structural and functional responses of a freshwater plankton community to acute copper stress, Environ. Pollut., 86, 259-266, (1994)
[24] Heffernan, J. M.; Smith, R. J.; Wahl, L. M., Perspectives on the basic reproductive ratio, J. R. Soc. Interface, 2, 281-293, (2005)
[25] Hilker, F. M.; Schmitz, K., Disease-induced stabilization of predator-prey oscillations, J. Theor. Biol., 255, 299-306, (2008) · Zbl 1400.92487
[26] Hite, J. L.; Penczykowski, R. M.; Shocket, M. S.; Strauss, A. T.; Orlando, P. A.; Duffy, M. A.; Cáceres, C. E.; Hall, S. R., Parasites destabilize host populations by shifting stage-structured interactions, Ecology, 97, 2, 439-449, (2016)
[27] Holmes, J. C., Parasites as threats to biodiversity in shrinking ecosystems, Biodivers. Conserv., 5, 975-983, (1996)
[28] Hurtado, P. J.; Hall, S. R.; Ellner, S. P., Infectious disease in consumer populations: dynamic consequences of resource-mediated transmission and infectiousness, Theor. Ecol., 7, 163-179, (2014)
[29] Ingersoll, C. G.; Winner, R. W., Effect on Daphnia pulex (de geer) of daily pulse exposures to copper or cadmium, Environ. Toxicol. Chem., 1, 321-327, (1982)
[30] Khan, R., 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, (1990)
[31] Knops, M.; Altenburger, R.; Segner, H., Alterations of physiological energetics, growth and reproduction of Daphnia magna under toxicant stress, Aquat. Toxicol., 53, 79-90, (2001)
[32] Koivisto, S.; Ketola, M.; Walls, M., Comparison of five cladoceran species in short-and long-term copper exposure, Hydrobiologia, 248, 125-136, (1992)
[33] Kooi, B.; Bontje, D.; Van Voorn, G.; Kooijman, S., Sublethal toxic effects in a simple aquatic food chain, Ecol. Modell., 212, 3-4, 304-318, (2008)
[34] Lafferty, K. D.; Holt, R. D., How should environmental stress affect the population dynamics of disease?, Ecol. Lett., 6, 654-664, (2003)
[35] Lafferty, K. D.; Kuris, A. M., How environmental stress affects the impacts of parasites, Limnol. Oceanogr., 44, 925-931, (1999)
[36] Lafferty, K. D.; Porter, J. W.; Ford, S. E., Are diseases increasing in the ocean?, Annu. Rev. Ecol. Evol. Syst., 35, 31-54, (2004)
[37] Lebrun, J. D.; Perret, M.; Geffard, A.; Gourlay-Francé, C., Modelling copper bioaccumulation in Gammarus pulex and alterations of digestive metabolism, Ecotoxicology, 21, 2022-2030, (2012)
[38] Luoma, S.; Rainbow, P., Metal contamination in aquatic environments: science and lateral management, (2008), Cambridge University Press, UK
[39] Luoma, S. N.; Rainbow, P. S., Why is metal bioaccumulation so variable? Biodynamics as a unifying concept, Environ. Sci. Technol., 39, 1921-1931, (2005)
[40] McCauley, E.; Murdoch, W. W.; Watson, S., Simple models and variation in plankton densities among lakes, Am. Nat., 132, 383-403, (1988)
[41] McCauley, E.; Nelson, W. A.; Nisbet, R. M., Small-amplitude cycles emerge from stage-structured interactions in Daphnia-algal systems, Nature, 455, 7217, 1240, (2008)
[42] Mertz, W., The essential trace elements, Science, 213, 1332-1338, (1981)
[43] Murdoch, W.; Nisbet, R.; McCauley, E.; DeRoos, A.; Gurney, W., Plankton abundance and dynamics across nutrient levels: tests of hypotheses, Ecology, 79, 1339-1356, (1998)
[44] O’Keefe, T. C.; Brewer, M. C.; Dodson, S. I., Swimming behavior of Daphnia: its role in determining predation risk, J. Plankton. Res., 20, 973-984, (1998)
[45] Prosnier, L.; Loreau, M.; Hulot, F. D., Modeling the direct and indirect effects of copper on phytoplankton zooplankton interactions, Aquat. Toxicol., 162, 73-81, (2015)
[46] Prosnier, L.; Médoc, V.; Loeuille, N., Parasitism effects on coexistence and stability within simple trophic modules, J. Theor. Biol., 458, 68-77, (2018) · Zbl 1406.92682
[47] Rainbow, P.; Luoma, S., Metal toxicity, uptake and bioaccumulation in aquatic invertebrates-modelling zinc in crustaceans, Aquat. Toxicol., 105, 455-465, (2011)
[48] Rana, S.; Samanta, S.; Bhattacharya, S.; Al-Khaled, K.; Goswami, A.; Chattopadhyay, J., The effect of nanoparticles on plankton dynamics: A mathematical model, Biosystems, 127, 28-41, (2015)
[49] Rigby, M.; Moret, Y., Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality, 129-142, (2000), Elsevier Science, Amsterdam
[50] Rinke, K.; Vijverberg, J., A model approach to evaluate the effect of temperature and food concentration on individual life-history and population dynamics of Daphnia, Ecol. Modell., 186, 326-344, (2005)
[51] Rip, J.; McCann, K., Cross-ecosystem differences in stability and the principle of energy flux, Ecol. Lett., 14, 8, 733-740, (2011)
[52] Rohr, J. R.; Raffel, T. R.; Sessions, S. K.; Hudson, P. J., Understanding the net effects of pesticides on amphibian trematode infections, Ecol. Appl., 18, 1743-1753, (2008)
[53] Rosenzweig, M. L.; MacArthur, R. H., Graphical representation and stability conditions of predator-prey interactions, Am. Nat., 97, 209-223, (1963)
[54] Sarkar, R. R.; Petrovskii, S. V.; Biswas, M.; Gupta, A.; Chattopadhyay, J., An ecological study of a marine plankton community based on the field data collected from bay of bengal, Ecol. Modell., 193, 589-601, (2006)
[55] Scheffer, M.; Rinaldi, S.; Kuznetsov, Y. A.; van Nes, E. H., Seasonal dynamics of Daphnia and algae explained as a periodically forced predator-prey system, Oikos, 80, 519-532, (1997)
[56] Scott, M. E., The impact of infection and disease on animal populations: implications for conservation biology, Conserv. Biol., 2, 40-56, (1988)
[57] Sullivan, B.; Buskey, E.; Miller, D.; Ritacco, P., Effects of copper and cadmium on growth, swimming and predator avoidance in Eurytemora affinis (copepoda), Mar. Biol., 77, 299-306, (1983)
[58] Untersteiner, H.; Kahapka, J.; Kaiser, H., Behavioural response of the cladoceran Daphnia magna STRAUS to sublethal copper stress-validation by image analysis, Aquat. Toxicol., 65, 435-442, (2003)
[59] Van Bressem, M.-F.; Raga, J. A.; Di Guardo, G.; Jepson, P. D.; Duignan, P. J.; Siebert, U.; Barrett, T.; de Oliveira Santos, M. C.; Moreno, I. B.; Siciliano, S., Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors, Dis. Aquat. Org., 86, 2, 143-157, (2009)
[60] WHO, Environmental health criteria, 200, (1998)
[61] Winner, R. W.; Farrell, M. P., Acute and chronic toxicity of copper to four species of Daphnia, J. Fish Res. Board Can., 33, 1685-1691, (1976)
[62] Wright, D. I.; O’Brien, W. J., Differential location of Chaoborus larvae and Daphnia by fish: the importance of motion and visible size, Am. Midl. Nat., 108, 68-73, (1982)
[63] Xiao, Y.; Van Den Bosch, F., The dynamics of an eco-epidemic model with biological control, Ecol. Modell., 168, 203-214, (2003)
[64] Yan, H.; Pan, G., Toxicity and bioaccumulation of copper in three green microalgal species, Chemosphere, 49, 471-476, (2002)
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