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Metal Toxicity Can Affect Dragonfly Nymphs and Ostracods Predation Rates and Food Selectivity: Ecological Implications on Food Webs

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Abstract

Predation is known to play a prominent role in maintaining ecosystem structure and functioning. Despite metals being known to potentially affect predation in aquatic ecosystems, few studies have been conducted, so far, with the aim of evaluating this interplay. In the present study, the effects of four metal salts (copper, cadmium, mercury, and manganese) on the feeding rates and food preference of the dragonfly Tramea cophisa and of the ostracod Chlamydotheca sp. were studied by performing laboratory ecotoxicity tests. Food preference was evaluated by offering four prey species to dragonfly nymphs and three to adult large ostracods. In general, the food preference of both predator species after being exposed to metal salts was not altered, compared with controls, but the feeding rate of T. cophisa decreased in comparison with controls, after exposure to each metal salt, except manganese. Contrastingly, predation rates of Chlamydotheca sp. increased after metal salt exposure. This difference in response can be explained by differences in life-history traits of these two organisms. Both species individuals preferred soft-bodied prey (Oligochaeta, Chironomidae) over water-dwelling crustaceans that are likely to be more difficult to prey upon. Tests evaluating the effects of metals and other chemicals on predation behavior may lead to a better understanding of biotic interactions that can be restricted by chemical stress, improving our understanding of possible food web disruptions underlying chemical stress.

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Data Availability

The datasets used during the current study are available from the corresponding author on reasonable request.

References

  • ABNT - Associação Brasileira de Normas Técnicas (2016). Aquatic ecotoxicology - acute toxicity - Test with Daphnia spp. (Cladocera, Crustacea). NBR 12713. ABNT, Rio de Janeiro.

  • Alzmann, N., Köhler, B., & Maier, G. (1999). Spatial distribution, food and activity of Gomphus pulchellus SELYS 1840 (Insecta; Odonata; Gomphidae) from a still water habitat. International Review of Hydrobiology, 84, 299–313.

    Google Scholar 

  • Anholt, B. (1992). Sex and habitat differences in feeding by an adult damselfly. Oikos, 65, 428–432.

    Article  Google Scholar 

  • Barnes, R.D. (1995). Zoologia de Invertebrados. 4ed. Ed. Roca, 1178 pp.

  • Buch, A. C., Brown, G. G., Correia, M. E. F., Lourençato, L. F., & Silva-Filho, E. V. (2017). Ecotoxicology of mercury in tropical forest soils: Impact on earthworms. Science of the Total Environment, 589, 222–231.

    Article  CAS  Google Scholar 

  • Campagna, A. F., Fracácio, R., Rodrigues, B. K., Eler, M. N., Verani, N. F., & Espíndola, E. L. G. (2008). Analyses of the sediment toxicity of Monjolinho River, São Carlos, São Paulo State, Brazil, using survey, growth and gill morphology of two fish species. Brazilian Archives of Biology and Technology, 51, 193–201.

    Article  CAS  Google Scholar 

  • Campbell, C. E. (1995). The influence of a predatory ostracod, Australocypris insularis, on zooplankton abundance and species composition in a saline lake. Hydrobiologia, 302, 229–239.

    Article  Google Scholar 

  • Clark, R. B. (1992). Marine pollution (p. 172). Clarendon Press.

    Google Scholar 

  • Corbi, J. J., Strixino, S. T., Santos, A. D., & Del Grande, M. (2006). Diagnóstico ambiental de metais e organoclorados em córregos adjacentes a áreas de cultivo de cana-de-açúcar (Estado de São Paulo, Brasil). Química Nova, 29, 61–65.

    Article  Google Scholar 

  • Corbi, J. J., Strixino, S. T., & Santos, A. D. (2008). Environmental evaluation of metals in sediments and dragonflies due to sugar cane cultivation in Neotropical streams. Water Air and Soil Pollution, 195, 325–333.

    Article  CAS  Google Scholar 

  • Corbi, J. J., Froehlich, C. G., Trivinho-Strixino, S., & Dos Santos, A. (2010). Bioaccumulation of metals in aquatic insects of streams located in areas with sugar cane cultivation. Química Nova, 33, 644–648.

    Article  CAS  Google Scholar 

  • Corbet, P. S. (1999). Dragonflies: Behavior and ecology. University Press.

    Google Scholar 

  • Correa, M., Coler, R. A., & Yin, C. M. (1985). Changes in oxygen consumption and nitrogen metabolism in the dragonfly Somatochlora cingulata exposed to aluminum in acid waters. Hydrobiologia, 121, 151–156.

    Article  CAS  Google Scholar 

  • Costa, C., Ide, S., & Simonka, C. E. (2006). Insetos imaturos: metamorfose e identificação. Ribeirão Preto: Holos. 249 pp.

  • Deschiens, R. (1954). Mécanisme de l’actionléthale de Cypridopsis hartwigi surles mollusques vecteurs des bilharzioses. Bulletin De La Société De Patholoie Exotique, 47, 399–401.

    CAS  Google Scholar 

  • Deschiens, R., Lamy, L., & Lamy, H. (1953). Sur un ostracode prédateur de Bullinset de Planorbes. Bulletin De La Société De Pathologie Exotique, 46, 956–958.

    CAS  Google Scholar 

  • Dornfeld, C. B., Rodgher, S., Negri, R. G., Espíndola, E. L. G., & Daam, M. A. (2018). Chironomus sancticaroli (Diptera, Chironomidae) as a sensitive tropical test species in laboratory bioassays evaluating metals (copper and cadmium) and field testing. 2018. Archives of Environmental Contamination and Toxicology, 76, 42–50.

    Article  CAS  Google Scholar 

  • Duleba, W., Coimbra, J. C. S., Petri, S., & Barbosa, C. F. (2005). Foraminíferos tecamebas e ostracodes recentes utilizados como bioindicadores em estudos ambientais brasileiros. In: C. R. G. Sousa, K. Suguio, M. Santos, & P. E. Oliveira (Eds.), Quaternário do Brasil. ABEQUA. Editora Holos, Ribeirão Preto, 176–201 pp.

  • Elmoor-Loureiro, L. M. A. (1997). Manual de identificação de cladóceros límnicos do Brasil. Brasília. Ed. Universitária. 156 pp.

  • Forrow, D. M., & Maltby, L. (2000). Toward a mechanistic understanding of contaminant-induced changes in detritus processing in streams: Direct and indirect effects on detritivore feeding. Environmental Toxicology and Chemistry, 19, 2100–2106.

    Article  CAS  Google Scholar 

  • Fulan, J. A., & Dos Anjos, M. R. D. (2015). Predation by Erythemis nymphs (Odonata) on Chironomidae (Diptera) and Elmidae (Coleoptera) in different conditions of habitat complexity. Acta Limnologica Brasiliensia, 27, 454–458.

    Article  Google Scholar 

  • Ganning, B. (1971). On the ecology of Heterocypris salinus, H. incongruens and Cypridopsis aculeata (Crustacea, Ostracoda) from Baltic brackish-water rockpools. Marine Biology, 8, 271–279.

    Article  Google Scholar 

  • Gerhardt, A., De Bisthoven, L. J., & Soares, A. M. V. M. (2004). Macroinvertebrate response to acid mine drainage: Community metrics and on-line behavioral toxicity bioassay. Environmental Pollution, 130, 263–274.

    Article  CAS  Google Scholar 

  • Gomes, D. F., Moreira, R. A., Sanches, N. A. O., Vale, C. A., Daam, M. A., Gorni, G. R., & Bastos, W. R. (2020). Dynamics of (total and methyl) mercury in sediment, fish, and crocodiles in an Amazonian Lake and risk assessment of fish consumption to the local population. Environmental Monitoring and Assessment, 192, 1–01.

    Article  CAS  Google Scholar 

  • Grainger, P., Christie, M., Thomas, G., Dole, S., Heck, D., Marshman, M., & Carey, M. (2017). Improving the quality of assessment by using a community of practice to explore the optimal construction of assessment rubrics. Reflective Practice, 18, 410–422.

    Article  Google Scholar 

  • Harrison, S. S. C., Bradley, D. C., & Harris, I. T. (2005). Uncoupling strong predator-prey interactions in streams: The role of marginal macrophytes. Oikos, 108, 443–448.

    Article  Google Scholar 

  • Hatch, A. C., & Burton, G. A. (1999). Phototoxicity of fluoranthene to two freshwater crustaceans, Hyalella azteca and Daphnia magna: Measures of feeding inhibition as a toxicological endpoint. Hydrobiologia, 400, 243–248.

    Article  CAS  Google Scholar 

  • Havel, J. E., & Talbott, B. L. (1995). Life history characteristics of the freshwater ostracod Cyprinotus incongruens and their application to toxicity testing. Ecotoxicology, 4, 206–218.

    Article  CAS  Google Scholar 

  • Hudspith, M., Reichelt-Brushett, A., & Harrison, P. L. (2017). Factors affecting the toxicity of trace metals to fertilization success in broadcast spawning marine invertebrates: A review. Aquatic Toxicology, 184, 1–13.

    Article  CAS  Google Scholar 

  • Irving, E. C., Baird, D. J., & Culp, J. M. (2003). Ecotoxicological responses of the mayfly Baetis tricaudatus to dietary and waterborne cadmium: Implications for toxicity testing. Environmental Toxicology and Chemistry, 22, 1058–1064.

    Article  CAS  Google Scholar 

  • Ivlev, V. S. (1961). Experimental ecology of the feeding of fishes (p. 302). Yale University Press.

    Google Scholar 

  • Khangarot, B. S., & Das, S. (2009). Acute toxicity of metals and reference toxicants to a freshwater ostracod, Cypris subglobosa Sowerby, 1840 and correlation to EC50 values of other test models. Journal of Hazardous Materials, 172, 641–649.

    Article  CAS  Google Scholar 

  • Khangarot, B. S., & Ray, P. K. (1987). Response of a freshwater ostracod (Cypris subglobosa Sowerby) exposed to copper at different pH levels. Acta Hydrochimica Et Hydrobiologica, 15, 553–558.

    Article  CAS  Google Scholar 

  • Kimbell, H. S., & Morrell, L. J. (2015). Turbidity influences individual and group level response to predation in guppies, Poecilia reticulata. Animal Behaviour, 103, 179–185.

    Article  Google Scholar 

  • Kotov, A. A., & Williams, J. L. (2000). Ilyocryptus spinifer Herrick 1882 (Anomopoda, Branchiopoda): A redescription based on North American material and designation of a neotype from Minnesota. Hydrobiologia, 428, 67–84.

    Article  Google Scholar 

  • Lailson-Brito, J., Jr., Dorneles, P. R., Da Silva, V. M., Martin, A. R., Bastos, W. R., Azevedo-Silva, C. E., & Malm, O. (2009). Dolphins as indicators of micropollutant trophic flow in Amazon Basin. Oecologia Brasiliensis, 12, 531–541.

    Google Scholar 

  • Lesch, V., & Bouwman, H. (2018). Adult dragonflies are indicators of environmental metallic elements. Chemosphere, 209, 654–665.

    Article  CAS  Google Scholar 

  • Lima, J. C. S., Neto, A. J. G., Andrade, D. P., Freitas, E. C., Moreira, R. A., Miguel, M., Daam, M. A., & Rocha, O. (2019). Acute toxicity of four metals to three tropical aquatic invertebrates: The dragonfly Tramea cophysa and the ostracods Chlamydotheca sp. and Strandesia trispinosa. Ecotoxicology and Environmental Safety, 180, 535–541.

    Article  CAS  Google Scholar 

  • Majumdar, T. N., & Gupta, A. (2012). Acute and chronic toxicity of copper on aquatic insect Chironomus ramosus from Assam, India. Journal of Environmental Biology, 33, 139–142.

    CAS  Google Scholar 

  • Martens, K. (1995). Recent non-marine Ostracoda. Workshop on Neotropical Aquatic Invertebrates University of São Paulo, Brazil, 31, 1–18.

    Google Scholar 

  • McGrinty, A. S. (1980). Survival, growth and variation growth of channel catfish fry and fingerlings. Alabama, 1980. (Thesis Doctoral) Auburn University.

  • McWilliam, R. A., & Baird, D. J. (2002). Application of post exposure feeding depression bioassays with Daphnia magna for assessment of toxic effluents in rivers. Environmental Toxicology and Chemistry, 21, 1462–1468.

    Article  CAS  Google Scholar 

  • Meisch, C. (2000). Freshwater Ostracoda of Western and Central Europe (p. 522). Spektrum Akademischer Verlag.

    Google Scholar 

  • Meyer, W., Harisch, G., & Sagredos, A. N. (1986). Biochemical and histochemical aspects of lead exposure in dragonfly larvae (Odonata: Anisoptera). Ecotoxicology and Environmental Safety, 11, 308–319.

    Article  CAS  Google Scholar 

  • Miguel, T. B., Oliveira-Junior, J. M. B., Ligeiro, R., & Juen, L. (2017). Odonata (Insecta) as a tool for the biomonitoring of environmental quality. Ecological Indicators, 81, 555–566.

    Article  CAS  Google Scholar 

  • Moiseenko, T. I., & Gashkina, N. A. (2018). Biogeochemistry of cadmium: Anthropogenic dispersion, bioaccumulation, and ecotoxicity. Geochemistry International, 5, 798–811.

    Article  Google Scholar 

  • Murugan, K., Benelli, G., Ayyappan, S., Dinesh, D., Panneerselvam, C., Nicoletti, M., & Suresh, U. (2015). Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus. Parasitology Research, 114, 2243–2253.

    Article  Google Scholar 

  • Oliveira, E., Takeuchi, S. S., & Cerutti, V. E. (2013). Assembleia de Larvas de Odonata (Insecta) em ambientes límnicos do Parque Estadual de Vila Velha, Paraná, Brasil. Estudos De Biologia, 35, 163–176.

    Article  Google Scholar 

  • Ottonello, D., & Romano, A. (2011). Ostracoda and Amphibia in temporary ponds: Who is the prey? Unexpected trophic relation in a Mediterranean freshwater habitat. Aquatic Ecology, 45, 55–62.

    Article  Google Scholar 

  • Pearson, W. H., Woodruff, D. L., Sugarman, P. C., & Olla, B. L. (1981). Effects of oiled sediment on predation on the littleneck clam, Protothaca staminea, by the Dungeness crab, Cancer magister. Estuarine, Coastal and Shelf Science, 13, 445–454.

    Article  CAS  Google Scholar 

  • Pinder, L. C. V. (1995). The habitats of chironomid larvae. In: P. D. Armitage, P. S. Cranston, & L. C. V. Pinder. Biology and ecology of non-biting midges. Chapman and Hall, London, U.K. 107–135 pp.

  • Pritchard, G. (1965). Prey capture by dragonfly larvae (Odonata; Anisoptera). Canadian Journal of Zoology, 43, 271–289.

    Article  Google Scholar 

  • Rockwood, J. P., Jones, D. S., & Coler, R. A. (1990). The effect of aluminum in soft water at low pH on oxygen consumption by the dragonfly Libellula julia Uhler. Hydrobiologia, 190, 55–59.

    Article  CAS  Google Scholar 

  • Ruiz, F., Abad, M., Bodergat, A. M., Carbonel, P., Rodríguez-Lázaro, J., González Regalado, M. L., Toscano, A., García, E. X., & Prenda, J. (2013). Freshwater ostracods as environmental tracers. International Journal of Environmental and Science Technology, 10, 1115–1128.

    Article  CAS  Google Scholar 

  • Shuhaimi-Othman, M., Yakub, N., Ramle, N. A., & Abas, A. (2011). Toxicity of metals to a freshwater ostracod: Stenocypris major. Journal of Toxicology, 2011, 1–8.

    Article  CAS  Google Scholar 

  • Sloff, W. (1983). Benthic macroinvertebrates and water quality assessment: Some toxicological considerations. Aquatic Toxicology, 4, 73–82.

    Article  Google Scholar 

  • Smith, G. M., & Weis, J. S. (1997). Predator-prey relationships in mummichogs (Fundulus heteroclitus (L.): Effects of living in a polluted environment. Journal of Experimental Marine Biology and Ecology, 209, 75–87.

    Article  Google Scholar 

  • Soares, C. M., Hayashi, C., & Faria, A. C. E. A. (2001). Influência da disponibilidade de presas, do contraste visual e do tamanho das larvas de Pantala sp. (Odonata, Insecta) sobre a predação de Simocephalus cerrulatus (Cladocera, Crustacea). Acta Scientarum. Biological Sciences, 23, 357–362.

    Google Scholar 

  • Soares, C. M., Hayashi, C., & Reidel, A. (2003). Predação de pós-larvas de curimba (Prochilodus lineatus, Valenciennes, 1836) por larvas de Odonata (Pantala sp., Fabricius, 1798) em diferentes tamanhos. Acta Scientarum. Biological Sciences, 25, 95–100.

    Google Scholar 

  • Sohn, I. G., & Kornicker, L. S. (1972). Predation of schistosomiasis vector snails by Ostracoda (Crustacea). Science, 175, 1258–1259.

    Article  CAS  Google Scholar 

  • Suhling, F., Martens, A., & Suhling, I. (2017). Long-distance dispersal in Odonata: Examples from arid Namibia. Austral Ecology, 42, 544–552.

    Article  Google Scholar 

  • Tave, D., Rezk, M., & Smitherman, R. O. (1990). Effect of body color of Oreochromis mossambicus (Peters) on predation by dragonfly nymphs. Aquaculture Research, 21, 157–161.

    Article  Google Scholar 

  • Thetmeyer, H., & Kils, U. (1995). To see and not be seen: The visibility of predator and prey with respect to feeding behaviour. Marine Ecology, 126, 1–8.

    Article  Google Scholar 

  • Thornton, I., Ramsey, M., & Atkinson, N. (1995). Metals in the global environment: Facts and misconceptions (p. 103). International Council on Metals and Environment (ICME).

    Google Scholar 

  • Tomazelli, O., Jr., Franco, G. M. S., Casaca, J. M., Munarini, A. C., & Dal Magro, J. (2011). Effect of the Melia azedarach L. on the predation of common carp fingerlings (Cyprinus carpio) by larvae of Neuraeschna (Odonata: Aeshnidae). Braz Journal of Aquatic Science & Technology, 15, 19–25.

    Article  Google Scholar 

  • Valente-Neto, F., De Oliveira Roque, F., Rodrigues, M. E., Juen, L., & Swan, C. M. (2016). Toward a practical use of Neotropical odonates as bioindicators: Testing congruence across taxonomic resolution and life stages. Ecological Indicators, 61, 952–959.

    Article  Google Scholar 

  • Van Stappen, G. (1996). Introduction, biology and ecology of Artemia. In: P. Lavens, & P. Sorgeloos (Eds). Manual on the Production and Use of Live Food for Aquaculture. FAO Fisheries Technical Paper, 295 pp.

  • Vannier, J., Abe, K., & Ikuta, K. (1998). Feeding in myodocopid ostracods: Functional morphology and laboratory observations from videos. Marine Biology, 132, 391–408.

    Article  Google Scholar 

  • Vieira, M. C., Torronteras, R., Córdoba, F., & Canalejo, A. (2012). Acute toxicity of manganese in goldfish Carassius auratus is associated with oxidative stress and organ specific antioxidant responses. Ecotoxicology and Environmental Safety, 78, 212–217.

    Article  CAS  Google Scholar 

  • Vogt, C., Hess, M., Nowak, C., Diogo, J. B., Oehlmann, J., & Oetken, M. (2010). Effects of cadmium on life-cycle parameters in a multi-generation study with Chironomus riparius following a pre-exposure of populations to two different tributyltin concentrations for several generations. Ecotoxicology, 19, 1174–1182.

    Article  CAS  Google Scholar 

  • Walker, C. H., Hopkin, S. P., Sibly, R. M., & Peakall, D. B. (2012). Principles of ecotoxicology (4th ed., p. 360). Taylor and Francis.

    Google Scholar 

  • Watts, M. M., & Pascoe, D. A. (2000). Comparative study of Chironomus riparius Meigen and Chironomus tentans Fabricius (Diptera: Chironomidae) in aquatic toxicity tests. Archives of Environmental Contamination and Toxicology, 39, 299–306.

    Article  CAS  Google Scholar 

  • Wayland, M., & Crosley, R. (2006). Selenium and other trace elements in aquatic insects in coalmine-affected streams in the Rocky Mountains of Alberta, Canada. Archives of Environmental Contamination and Toxicology, 50, 511–522.

    Article  CAS  Google Scholar 

  • Weis, J. S., Samson, J., Zhou, T., Skurnick, J., & Weis, P. (2001). Prey capture ability of mummichogs (Fundulus heteroclitus) as a behavioral biomarker for contaminants in estuarine systems. Canadian Journal of Fisheries and Aquatic Science, 58, 1442–1452.

    Article  CAS  Google Scholar 

  • Weis, J. S., Samson, J., Zhou, T., Skurnick, J., & Weis, P. (2003). Evaluating prey capture by larval mummichogs (Fundulus heteroclitus) as a potential biomarker for contaminants. Marine Environmental Research, 55, 27–38.

    Article  CAS  Google Scholar 

  • Williams, M., Perrier, V., Bennett, C., & Hearing, T. (2015). Ostracods: The ultimate survivors. Geology Today, 31, 193–200.

    Article  Google Scholar 

  • Wilkinson, I. P., Wilby, P. R., Williams, M., Siveter, D. J., & Vannier, J. (2007). Ostracod carnivory through time. In: Elewa ATM (Ed.). Predation in organisms: a distinct phenomenon. Springer Berlin, Heidelberg., 39–57 pp.

  • Yuan, D., Huang, L., Zeng, L., & Liu, S. (2017). Acute toxicity of mercury chloride (HgCl2) and cadmium chloride (CdCl2) on the behavior of freshwater fish, Percocypris pingi. International Journal of Aquaculture Fisheries and Science, 7, 66–70.

    Google Scholar 

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Acknowledgements

The authors are indebted to the Brazilian National Research Council (CNPq, Process: 140400/2015-0) and CAPES for scholarships to the first author in different periods, and to Dr. Norma Luiza Würdig from the Federal University of Rio Grande do Sul, RS, Brazil, for the taxonomic identification of the Ostracoda species. R.A.M. has a postdoctoral fellowship from FAPESP (grant no. 2017/24126-4). This work was also supported by the Portuguese government (FCT) through a postdoc grant for M. Daam (SFRH/BPD/109199/ 2015) and the research unit UID/AMB/04085/2013 (CENSE). The work was also partially supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), Finance Code 001.

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dos Santos Lima, J., Moreira, R., Neto, A. et al. Metal Toxicity Can Affect Dragonfly Nymphs and Ostracods Predation Rates and Food Selectivity: Ecological Implications on Food Webs. Water Air Soil Pollut 232, 288 (2021). https://doi.org/10.1007/s11270-021-05248-3

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