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Temperature modulates the interaction between fungicide pollution and disease: evidence from a Daphnia-microparasitic yeast model

  • Ana P. Cuco (a1) (a2), Bruno B. Castro (a3), Fernando Gonçalves (a1) (a2), Justyna Wolinska (a4) (a5) and Nelson Abrantes (a2) (a6)...


Temperature is expected to modulate the responses of organisms to stress. Here, we aimed to assess the influence of temperature on the interaction between parasitism and fungicide contamination. Specifically, using the cladoceran Daphnia as a model system, we explored the isolated and interactive effects of parasite challenge (yeast Metschnikowia bicuspidata) and exposure to fungicides (copper sulphate and tebuconazole) at two temperatures (17 and 20 °C), in a fully factorial design. Confirming a previous study, M. bicuspidata infection and copper exposure caused independent effects on Daphnia life history, whereas infection was permanently suppressed with tebuconazole exposure. Here, we show that higher temperature generally increased the virulence of the parasite, with the hosts developing signs of infection earlier, reproducing less and dying at an earlier age. These effects were consistent across copper concentrations, whereas the joint effects of temperature (which enhanced the difference between non-infected and infected hosts) and the anti-parasitic action of tebuconazole resulted in a more pronounced parasite × tebuconazole interaction at the higher temperature. Thus, besides independently influencing parasite and contaminant effects, the temperature can act as a modulator of interactions between pollution and disease.


Corresponding author

Author for correspondence: Bruno B. Castro, E-mail:


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Agha, R, Saebelfeld, M, Manthey, C, Rohrlack, T and Wolinska, J (2016) Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia). Scientific Reports 6, 35039.
Álvarez-Pérez, S, de Vega, C, Pozo, MI, Lenaerts, M, Van Assche, A, Herrera, CM, Jacquemyn, H and Lievens, B (2015) Nectar yeasts of the Metschnikowia clade are highly susceptible to azole antifungals widely used in medicine and agriculture. FEMS Yeast Research 16, 115.
Bereswill, R, Golla, B, Streloke, M and Schulz, R (2012) Entry and toxicity of organic pesticides and copper in vineyard streams: erosion rills jeopardise the efficiency of riparian buffer strips. Agriculture, Ecosystems & Environment 146, 8192.
Blanar, CA, MacLatchy, DL, Kieffer, JD and Munkittrick, KR (2010) Exposure to a mixture of zinc and copper decreases survival and fecundity of Discocotyle sagittata (Leuckart) parasitizing juvenile Atlantic salmon, Salmo salar L. Bulletin of Environmental Contamination and Toxicology 84, 692697.
Burns, CW (1969) Relation between filtering rate, temperature and body size in four species of Daphnia. Limnology and Oceanography 14, 693700.
Buser, CC, Jansen, M, Pauwels, K, De Meester, L and Spaak, P (2012a) Combined exposure to parasite and pesticide causes increased mortality in the water flea Daphnia. Aquatic Ecology 46, 261268.
Buser, CC, Spaak, P and Wolinska, J (2012b) Disease and pollution alter Daphnia taxonomic and clonal structure in experimental assemblages. Freshwater Biology 57, 18651874.
Caceres, CE, Hall, SR, Duffy, MA, Tessier, AJ, Helmle, C and MacIntyre, S (2006) Physical structure of lakes constrains epidemics in Daphnia populations. Ecology 87, 14381444.
Civitello, DJ, Forys, P, Johnson, AP and Hall, SR (2012) Chronic contamination decreases disease spread: a Daphnia-fungus-copper case study. Proceedings of the Royal Society B: Biological Sciences 279, 31463153.
Coors, A, Decaestecker, E, Jansen, M and De Meester, L (2008) Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 117, 18401846.
Cuco, AP, Abrantes, N, Gonçalves, F, Wolinska, J and Castro, BB (2016) Toxicity of two fungicides in Daphnia: is it always temperature-dependent? Ecotoxicology 25, 13761389.
Cuco, AP, Abrantes, N, Gonçalves, F, Wolinska, J and Castro, BB (2017) Interplay between fungicides and parasites: Tebuconazole, but not copper, suppresses infection in a Daphnia-Metschnikowia experimental model. PLOS ONE 12, e0172589.
Dallas, T and Drake, JM (2016) Fluctuating temperatures alter environmental pathogen transmission in a Daphnia-pathogen system. Ecology and Evolution 6, 79317938.
Dean, R, Van Kan, JAL, Pretorius, ZA, Hammond-Kosack, KE, Di Pietro, A, Spanu, PD, Rudd, JJ, Dickman, M, Kahmann, R, Ellis, J and Foster, GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13, 414430.
Delcour, I, Spanoghe, P and Uyttendaele, M (2014) Literature review: impact of climate change on pesticide use. Food Research International 68, 715.
Dietrich, JP, Van Gaest, AL, Strickland, SA and Arkoosh, MR (2014) The impact of temperature stress and pesticide exposure on mortality and disease susceptibility of endangered Pacific salmon. Chemosphere 108, 353359.
Dighton, J (2016) Fungi in Ecosystem Processes, 2nd edn. Boca Raton, FL: CRC Press, Taylor & Francis Group.
Duffy, MA and Hall, SR (2008) Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. American Naturalist 171, 499510.
Duffy, MA and Sivars-Becker, L (2007) Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10, 4453.
Duffy, MA, Hall, SR, Caceres, CE, Ives, AR, Cáceres, CE, Ives, AR and Caceres, CE (2009) Rapid evolution, seasonality, and the termination of parasite epidemics. Ecology 90, 14411448.
Duffy, MA, Housley, JM, Penczykowski, RM, Caceres, CE and Hall, SR (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Functional Ecology 25, 945953.
Duncan, AB and Little, TJ (2007) Parasite-driven genetic change in a natural population of Daphnia. Evolution 61, 796803.
Ebert, D (2005) Ecology, Epidemiology, and Evolution of Parasitism in Daphnia. Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information.
Fischer, BB, Pomati, F and Eggen, RIL (2013) The toxicity of chemical pollutants in dynamic natural systems: the challenge of integrating environmental factors and biological complexity. The Science of the Total Environment 449, 253259.
Frenken, T, Velthuis, M, de Senerpont Domis, LN, Stephan, S, Aben, R, Kosten, S, van Donk, E and Van de Waal, DB (2016) Warming accelerates termination of a phytoplankton spring bloom by fungal parasites. Global Change Biology 22, 299309.
Gallana, M, Ryser-Degiorgis, MP, Wahli, T and Segner, H (2013) Climate change and infectious diseases of wildlife: altered interactions between pathogens, vectors and hosts. Current Zoology 59, 427437.
Garbutt, JS, Scholefield, JA, Vale, PF and Little, TJ (2014) Elevated maternal temperature enhances offspring disease resistance in Daphnia magna. Functional Ecology 28, 424431.
Gleason, FH, Jephcott, TG, Küpper, FC, Gerphagnon, M, Sime-Ngando, T, Karpov, SA, Guillou, L and van Ogtrop, FF (2015) Potential roles for recently discovered chytrid parasites in the dynamics of harmful algal blooms. Fungal Biology Reviews 29, 2033.
Gozlan, RE, Marshall, WL, Lilje, O, Jessop, CN, Gleason, FH and Andreou, D (2014) Current ecological understanding of fungal-like pathogens of fish: what lies beneath? Frontiers in Microbiology 5, 116.
Grossart, HP, Wurzbacher, C, James, TY and Kagami, M (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecology 19, 2838.
Hall, SR, Tessier, AJ, Duffy, MA, Huebner, M and Cáceres, CE (2006) Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics. Ecology 87, 16841695.
Hall, SR, Becker, CR, Simonis, JL, Duffy, MA, Tessier, AJ and Caceres, CE (2009) Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90, 791801.
Hall, SR, Becker, CR, Duffy, MA and Caceres, CE (2011) Epidemic size determines population-level effects of fungal parasites on Daphnia hosts. Oecologia 166, 833842.
Hall, MD, Vettiger, A and Ebert, D (2013) Interactions between environmental stressors: the influence of salinity on host-parasite interactions between Daphnia magna and Pasteuria ramosa. Oecologia 171, 789796.
Hanlon, SM, Kerby, JL and Parris, MJ (2012) Unlikely remedy: fungicide clears infection from pathogenic fungus in larval southern leopard frogs (Lithobates sphenocephalus). PLoS ONE 7, 18.
Hanlon, SM, Lynch, KJ, Kerby, JL and Parris, MJ (2015) The effects of a fungicide and chytrid fungus on anuran larvae in aquatic mesocosms. Environmental Science and Pollution Research 22, 1292912940.
Hesse, O, Engelbrecht, W, Laforsch, C and Wolinska, J (2012) Fighting parasites and predators: how to deal with multiple threats? BMC Ecology 12, 12.
Heugens, EHW, Hendriks, AJ, Dekker, T, van Straalen, NM and Admiraal, W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Critical Reviews in Toxicology 31, 247284.
Holmstrup, M, Bindesbøl, A-M, Oostingh, GJ, Duschl, A, Scheil, V, Köhler, H-R, Loureiro, S, Soares, AMVM, Ferreira, ALG, Kienle, C, Gerhardt, A, Laskowski, R, Kramarz, PE, Bayley, M, Svendsen, C and Spurgeon, DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Science of The Total Environment 408, 37463762.
IPCC (2014). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland: Core Writ. IPCC.
Jephcott, TG, Alves-de-Souza, C, Gleason, FH, van Ogtrop, FF, Sime-Ngando, T, Karpov, SA and Guillou, L (2016) Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Fungal Ecology 19, 4758.
Johnson, PTJ, Chase, JM, Dosch, KL, Hartson, RB, Gross, JA, Larson, DJ, Sutherland, DR and Carpenter, SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences of the United States of America 104, 1578115786.
Jokela, J, Dybdahl, MF and Lively, CM (2009) The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. The American Naturalist 174, S43S53.
Kahle, M, Buerge, IJ, Hauser, A, Müller, MD and Poiger, T (2008) Azole fungicides: occurrence and fate in wastewater and surface waters. Environmental Science & Technology 42, 71937200.
Kekäläinen, J, Lai, YT, Vainikka, A, Sirkka, I and Kortet, R (2014) Do brain parasites alter host personality? Experimental study in minnows. Behavioral Ecology and Sociobiology 68, 197204.
Kelly, DW, Poulin, R, Tompkins, DM and Townsend, CR (2010) Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. Journal of Applied Ecology 47, 498504.
Lass, S and Ebert, D (2006) Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proceedings of the Royal Society B-Biological Sciences 273, 199206.
Lohr, JN, Yin, M and Wolinska, J (2010) Prior residency does not always pay off – co-infections in Daphnia. Parasitology 137, 14931500.
Manavathu, EK, Cutright, JL and Chandrasekar, PH (1998) Organism-dependent fungicidal activities of azoles. Antimicrobial Agents and Chemotherapy 42, 30183021.
Marcogliese, DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Revue scientifique et technique (International Office of Epizootics) 27, 467484.
Marcogliese, DJ and Pietrock, M (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27, 123130.
McCallum, H (2000). Population Parameters: Estimation for Ecological Models. Oxford: Blackwell Science Ltd. doi:10.1002/9780470757468.
Meyer, JS, Ingersoll, CG, McDonald, LL and Boyce, MS (1986) Estimating uncertainty in population growth rates: Jackknife vs. Bootstrap techniques. Ecology 67, 1156.
Mitchell, SE, Rogers, ES, Little, TJ and Read, AF (2005) Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution; International Journal of Organic Evolution 59, 7080.
Noyes, PD, McElwee, MK, Miller, HD, Clark, BW, Van Tiem, LA, Walcott, KC, Erwin, KN and Levin, ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environment International 35, 971986.
OECD, (2012) Daphnia magna Reproduction Test. OECD Test Guidelines for Testing of Chemicals - Guideline 211. Paris: Organization for the Economic Co-operation and Development.
Scherer, C, Seeland, A, Oehlmann, J and Müller, R (2013) Interactive effects of xenobiotic, abiotic and biotic stressors on Daphnia pulex – results from a multiple stressor experiment with a fractional multifactorial design. Aquatic Toxicology 138–139, 105115.
Schoebel, CN, Tellenbach, C, Spaak, P and Wolinska, J (2011) Temperature effects on parasite prevalence in a natural hybrid complex. Biology Letters 7, 108111.
Seeland, A, Oehlmann, J and Müller, R (2012) Aquatic ecotoxicity of the fungicide pyrimethanil: effect profile under optimal and thermal stress conditions. Environmental Pollution (Barking, Essex: 1987) 168, 161169.
Vale, PF, Stjernman, M and Little, TJ (2008) Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology 21, 14181427.
Wolinska, J and King, KC (2009) Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236244.
Wolinska, J and Spaak, P (2009) The cost of being common: evidence from natural Daphnia populations. Evolution 63, 18931901.
Wolinska, J, Seda, J, Koerner, H, Smilauer, P and Petrusek, A (2011) Spatial variation of Daphnia parasite load within individual water bodies. Journal of Plankton Research 33, 12841294.
Yin, M, Laforsch, C, Lohr, JN and Wolinska, J (2011) Predator-induced defense makes Daphnia more vulnerable to parasites. Evolution; International Journal of Organic Evolution 65, 14821488.


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Temperature modulates the interaction between fungicide pollution and disease: evidence from a Daphnia-microparasitic yeast model

  • Ana P. Cuco (a1) (a2), Bruno B. Castro (a3), Fernando Gonçalves (a1) (a2), Justyna Wolinska (a4) (a5) and Nelson Abrantes (a2) (a6)...


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