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Ecotoxicology

, Volume 25, Issue 7, pp 1376–1389 | Cite as

Toxicity of two fungicides in Daphnia: is it always temperature-dependent?

  • Ana P. Cuco
  • Nelson Abrantes
  • Fernando Gonçalves
  • Justyna Wolinska
  • Bruno B. Castro
Article

Abstract

The joint effect of increasing temperature and pollution on aquatic organisms is important to understand and predict, as a combination of stressors might be more noxious when compared to their individual effects. Our goal was to determine the sensitivity of a model organism (Daphnia spp.) to contaminants at increasing temperatures, allowing prior acclimation of the organisms to the different temperatures. Prior to exposure, two Daphnia genotypes (Daphnia longispina species complex) were acclimated to three temperatures (17, 20, and 23 °C). Afterwards, a crossed design was established using different exposure temperatures and a range of concentrations of two common fungicides (tebuconazole and copper). Daphnia life history parameters were analysed in each temperature × toxicant combination for 21 days. Temperature was the most influencing factor: Daphnia reproduced later and had lower fecundity at 17 °C than at 20 and 23 °C. Both copper and tebuconazole also significantly reduced the fecundity and survival of Daphnia at environmentally-relevant concentrations. Temperature-dependence was found for both toxicants, but the response pattern was endpoint- and genotype-specific. The combination of contaminant and high temperature often had severe effects on survival. However, unlike some literature on the subject, our results do not support the theory that increasing temperatures consistently foment increasing reproductive toxicity. The absence of a clear temperature-dependent toxicity pattern may result from the previous acclimation to the temperature regime. However, a proper framework is lacking to compare such studies and to avoid misleading conclusions for climate change scenarios.

Keywords

Copper sulphate Tebuconazole Temperature rise Daphnia Acclimation 

Notes

Acknowledgments

Authors thank Mark Phillipo for linguistic help.

Funding

This work was supported by European funds through COMPETE2020 (European Regional Development Fund) and by national funds through the Portuguese Science Foundation (FCT I.P.) within the strategic programmes UID/AMB/50017/2013 (CESAM) and UID/BIA/04050/2013 (CBMA), as well as by the research project VITAQUA (PTDC/AAC-AMB/112438/2009). Ana P. Cuco and Nelson Abrantes are individual recipients of, respectively, a PhD Grant (SFRH/BD/81661/2011) and a researcher contract (IF/01198/2014) from FCT.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study did not involve any research conducted on human participants. No specific permissions were necessary, because the existing legislation on the welfare of experimental animals is not applicable and the study did not involve the collection of endangered or protected species.

References

  1. Antunes SC, Castro BB, Goncalves F (2003) Chronic responses of different clones of Daphnia longispina (field and ephippia) to different food levels. Acta Oecol 24:S325–S332. doi: 10.1016/s1146-609x(03)00026-2 CrossRefGoogle Scholar
  2. Antunes SC, Castro BB, Goncalves F (2004) Effect of food level on the acute and chronic responses of daphnids to lindane. Environ Pollut 127:367–375. doi: 10.1016/j.envpol.2003.08.015 CrossRefGoogle Scholar
  3. Balbus JM, Boxall AB, Fenske R, McKone TE, Zeise L (2013) Implications of global climate change for the assessment and management of human health risks of chemicals in the natural environment. Environ Toxicol Chem 32:62–78. doi: 10.1002/etc.2046 CrossRefGoogle Scholar
  4. Bates B, Kundzewicz Z, Wu S, Palutikof J (2008) Climate change and water: technical paper of the intergovernmental panel on climate change. IPCC Secretariat, GenevaGoogle Scholar
  5. Berenzen N, Lentzen-Godding A, Probst M, Schulz H, Schulz R, Liess M (2005) A comparison of predicted and measured levels of runoff-related pesticide concentrations in small lowland streams on a landscape level. Chemosphere 58:683–691. doi: 10.1016/j.chemosphere.2004.05.009 CrossRefGoogle Scholar
  6. Bereswill R, Golla B, Streloke M, Schulz R (2012) Entry and toxicity of organic pesticides and copper in vineyard streams: erosion rills jeopardise the efficiency of riparian buffer strips. Agric Ecosyst Environ 146:81–92. doi: 10.1016/j.agee.2011.10.010 CrossRefGoogle Scholar
  7. Bloomfield JP, Williams RJ, Gooddy DC, Cape JN, Guha P (2006) Impacts of climate change on the fate and behaviour of pesticides in surface and groundwater—a UK perspective. Sci Total Environ 369:163–177. doi: 10.1016/j.scitotenv.2006.05.019 CrossRefGoogle Scholar
  8. Boersma M, De Meester L, Spaak P (1999) Environmental stress and local adaptation in Daphnia magna. Limnol Oceanogr 44:393–402CrossRefGoogle Scholar
  9. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. doi: 10.1890/03-9000 CrossRefGoogle Scholar
  10. Brucet S, Boix D, Quintana XD, Jensen E, Nathansen LW, Trochine C, Meerhoff M, Gascón S, Jeppesen E (2010) Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnol Oceanogr 55:1697–1711. doi: 10.4319/lo.2010.55.4.1697 CrossRefGoogle Scholar
  11. Buser CC, Spaak P, Wolinska J (2012) Disease and pollution alter Daphnia taxonomic and clonal structure in experimental assemblages. Freshw Biol 57:1865–1874. doi: 10.1111/j.1365-2427.2012.02846.x CrossRefGoogle Scholar
  12. Castro BB, Consciência S, Gonçalves F (2007) Life history responses of Daphnia longispina to mosquitofish (Gambusia holbrooki) and pumpkinseed (Lepomis gibbosus) kairomones. Hydrobiologia 594:165–174. doi: 10.1007/s10750-007-9074-5 CrossRefGoogle Scholar
  13. Cerejeira MJ, Viana P, Batista S, Pereira T, Silva E, Valério MJ, Silva A, Ferreira M, Silva-Fernandes AM (2003) Pesticides in Portuguese surface and ground waters. Water Res 37:1055–1063CrossRefGoogle Scholar
  14. Chopelet J, Blier PU, Dufresne F (2008) Plasticity of growth rate and metabolism in Daphnia magna populations from different thermal habitats. J Exp Zool Ecol Genet Physiol 309:553–562. doi: 10.1002/jez.488 CrossRefGoogle Scholar
  15. Coors A, De Meester L (2008) Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna. J Appl Ecol 45:1820–1828. doi: 10.1111/j.1365-2664.2008.01566.x CrossRefGoogle Scholar
  16. Dang CK, Schindler M, Chauvet E, Gessner MO (2009) Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition. Ecology 90:122–131. doi: 10.1890/07-1974.1 CrossRefGoogle Scholar
  17. De Meester L, Van Doorslaer W, Geerts A, Orsini L, Stoks R (2011) Thermal genetic adaptation in the water flea Daphnia and its impact: an evolving metacommunity approach. Integr Comp Biol 51:703–718. doi: 10.1093/icb/icr027 CrossRefGoogle Scholar
  18. Engert A, Chakrabarti S, Saul N, Bittner M, Menzel R, Steinberg CEW (2013) Interaction of temperature and an environmental stressor: Moina macrocopa responds with increased body size, increased lifespan, and increased offspring numbers slightly above its temperature optimum. Chemosphere 90:2136–2141. doi: 10.1016/j.chemosphere.2012.10.099 CrossRefGoogle Scholar
  19. Ferreira ALG, Serra P, Soares AMVM, Loureiro S (2010) The influence of natural stressors on the toxicity of nickel to Daphnia magna. Environ Sci Pollut Res 17:1217–1229. doi: 10.1007/s11356-010-0298-y CrossRefGoogle Scholar
  20. Fischer JM, Olson MH, Williamson CE, Everhart JC, Hogan PJ, Mack JA, Rose KC, Saros JE, Stone JR, Vinebrooke RD (2011) Implications of climate change for Daphnia in alpine lakes: predictions from long-term dynamics, spatial distribution, and a short-term experiment. Hydrobiologia 676:263–277. doi: 10.1007/s10750-011-0888-9 CrossRefGoogle Scholar
  21. Fischer BB, Pomati F, Eggen RIL (2013) The toxicity of chemical pollutants in dynamic natural systems: the challenge of integrating environmental factors and biological complexity. Sci Total Environ 449:253–259. doi: 10.1016/j.scitotenv.2013.01.066 CrossRefGoogle Scholar
  22. Forbes V, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556CrossRefGoogle Scholar
  23. Garric J, Migeon B, Vindimian E (1990) Lethal effects of draining on brown trout. a predictive model based on field and laboratory studies. Water Res 24:59–65. doi: 10.1016/0043-1354(90)90065-E CrossRefGoogle Scholar
  24. Gouveia C, Liberato M, DaCamara C, Trigo R, Ramos A (2011) Modelling past and future wine production in the Portuguese douro valley. Clim Res 48:349–362. doi: 10.3354/cr01006 CrossRefGoogle Scholar
  25. Green JW (2014) Power and control choice in aquatic experiments with solvents. Ecotoxicol Environ Saf 102:142–146. doi: 10.1016/j.ecoenv.2014.01.024 CrossRefGoogle Scholar
  26. Green J, Wheeler JR (2013) The use of carrier solvents in regulatory aquatic toxicology testing: practical, statistical and regulatory considerations. Aquat Toxicol 144–145:242–249. doi: 10.1016/j.aquatox.2013.10.004 CrossRefGoogle Scholar
  27. Hanazato T (2001) Pesticide effects on freshwater zooplankton: an ecological perspective. Environ Pollut 112:1–10CrossRefGoogle Scholar
  28. Heugens EH, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247–284CrossRefGoogle Scholar
  29. Heugens E, Jager T, Creyghton R, Kraak M, Hendriks A, van Straalen N, Admiraal W (2003) Temperature-dependent effects of cadmium on Daphnia magna: accumulation versus sensitivity. Environ Sci Technol 37(10):2145–2151CrossRefGoogle Scholar
  30. Heugens E, Tokkie L, Kraak M, Hendriks A, van Straalen N, Admiraal W (2006) Population growth of Daphnia magna under multiple stress conditions: joint effects of temperature, food, and cadmium. Environ Toxicol Chem 25:1399–1407CrossRefGoogle Scholar
  31. 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, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762CrossRefGoogle Scholar
  32. IPCC (2014a) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University, CambridgeGoogle Scholar
  33. IPCC (2014b) 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, Core Writing Team, R.K. Pachauri L.A. Meyer (eds.) IPCC, GenevaGoogle Scholar
  34. Jansen M, Coors A, Stoks R, De Meester L (2011a) Evolutionary ecotoxicology of pesticide resistance: a case study in Daphnia. Ecotoxicology 20:543–551. doi: 10.1007/s10646-011-0627-z CrossRefGoogle Scholar
  35. Jansen M, De Meester L, Cielen A, Buser CC, Stoks R (2011b) The interplay of past and current stress exposure on the water flea Daphnia. Funct Ecol 25:974–982. doi: 10.1111/j.1365-2435.2011.01869.x CrossRefGoogle Scholar
  36. Kegley SE, Hill BR, Orme S, Choi, AH, (2014). PAN Pesticide Database. Pestic. Action Netw., North America Oakland URL http://www.pesticideinfo.org
  37. Kim J, Park J, Kim PG, Lee C, Choi K, Choi K (2010) Implication of global environmental changes on chemical toxicity-effect of water temperature, pH, and ultraviolet B irradiation on acute toxicity of several pharmaceuticals in Daphnia magna. Ecotoxicology 19:662–669. doi: 10.1007/s10646-009-0440-0 CrossRefGoogle Scholar
  38. Knillmann S, Stampfli NC, Noskov YA, Beketov MA, Liess M (2013) Elevated temperature prolongs long-term effects of a pesticide on Daphnia spp. due to altered competition in zooplankton communities. Glob Chang Biol 19:1598–1609. doi: 10.1111/gcb.12151 CrossRefGoogle Scholar
  39. Komárek M, Cadková E, Chrastný V, Bordas F, Bollinger J-C (2010) Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environ Int 36:138–151. doi: 10.1016/j.envint.2009.10.005 CrossRefGoogle Scholar
  40. Krienitz L, Bock C, Nozaki H, Wolf M (2011) SSU rRNA gene phylogeny of morphospecies affiliated to the bioassay alga “Selenastrum capricornutum” recovered the polyphyletic origin of crescent-shaped chlorophyta1. J Phycol 47:880–893. doi: 10.1111/j.1529-8817.2011.01010.x CrossRefGoogle Scholar
  41. Lagerspetz KYH, Vainio LA (2006) Thermal behaviour of crustaceans. Biol Rev Camb Philos Soc 81:237–258. doi: 10.1017/S1464793105006998 CrossRefGoogle Scholar
  42. Lampert W (2006) Daphnia: model herbivore, predator and prey. Polish J Ecol 54:607–620Google Scholar
  43. Lewis KA, Tzilivakis J, Warner DJ, Green A (2016) An international database for pesticide risk assessments and management. Hum Ecol Risk Assess 22:1050–1064. doi: 10.1080/10807039.2015.1133242 CrossRefGoogle Scholar
  44. Loureiro C, Castro BB, Pereira JL, Gonçalves F (2011) Performance of standard media in toxicological assessments with Daphnia magna: chelators and ionic composition versus metal toxicity. Ecotoxicology 20:139–148. doi: 10.1007/s10646-010-0565-1 CrossRefGoogle Scholar
  45. Loureiro C, Castro BB, Cuco AP, Pedrosa MA, Gonçalves F (2013) Life-history responses of salinity-tolerant and salinity-sensitive lineages of a stenohaline cladoceran do not confirm clonal differentiation. Hydrobiologia 702:73–82. doi: 10.1007/s10750-012-1308-5 CrossRefGoogle Scholar
  46. Loureiro C, Cuco AP, Claro MT, Santos JI, Pedrosa MA, Gonçalves F, Castro BB (2015) Progressive acclimation alters interaction between salinity and temperature in experimental Daphnia populations. Chemosphere 139:126–132. doi: 10.1016/j.chemosphere.2015.05.081 CrossRefGoogle Scholar
  47. Luoto TP, Nevalainen L (2013) Climate change impacts on zooplankton and benthic communities in Lake Unterer Giglachsee (Niedere Tauern Alps, Austria). Int Rev Hydrobiol 98:80–88. doi: 10.1002/iroh.201301461 CrossRefGoogle Scholar
  48. McCallum H (1999) Rate of increase of a population. In: Population parameters: estimation for ecological models. Blackwell Science Ltd, Oxford. doi: 10.1002/9780470757468.ch5
  49. Messiaen M, De Schamphelaere KAC, Muyssen BTA, Janssen CR (2010) The micro-evolutionary potential of Daphnia magna population exposed to temperature and cadmium stress. Ecotoxicol Environ Saf 73:1114–1122. doi: 10.1016/j.ecoenv.2010.05.006 CrossRefGoogle Scholar
  50. Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology 67:1156. doi: 10.2307/1938671 CrossRefGoogle Scholar
  51. Meyer JS, Ingersoll CG, McDonald LL (1987) Sensitivity analysis of population growth rates estimated from cladoceran chronic toxicity tests. Environ Toxicol Chem 6:115–126. doi: 10.1002/etc.5620060206 CrossRefGoogle Scholar
  52. Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61. doi: 10.1002/etc.2045 CrossRefGoogle Scholar
  53. Moreira L, (2013). Exportação de nutrientes e pesticidas em áreas vitícolas. Master Thesis, University of AveiroGoogle Scholar
  54. Muyssen BTA, Messiaen M, Janssen CR (2010) Combined cadmium and temperature acclimation in Daphnia magna: physiological and sub-cellular effects. Ecotoxicol Environ Saf 73:735–742. doi: 10.1016/j.ecoenv.2009.12.018 CrossRefGoogle Scholar
  55. Neves M, Castro BB, Vidal T, Vieira R, Marques JC, Coutinho JAP, Gonçalves F, Gonçalves AMM (2015) Biochemical and populational responses of an aquatic bioindicator species, Daphnia longispina, to a commercial formulation of a herbicide (Primextra® Gold TZ) and its active ingredient (S-metolachlor). Ecol. Indic. 53:220–230. doi: 10.1016/j.ecolind.2015.01.031 CrossRefGoogle Scholar
  56. Nielsen DL, Brock MA (2009) Modified water regime and salinity as a consequence of climate change: prospects for wetlands of Southern Australia. Clim Change 95:523–533. doi: 10.1007/s10584-009-9564-8 CrossRefGoogle Scholar
  57. Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986. doi: 10.1016/j.envint.2009.02.006 CrossRefGoogle Scholar
  58. Ochoa-Acuña HG, Bialkowski W, Yale G, Hahn L (2009) Toxicity of soybean rust fungicides to freshwater algae and Daphnia magna. Ecotoxicology 18:440–446. doi: 10.1007/s10646-009-0298-1 CrossRefGoogle Scholar
  59. OECD 2012. Test No. 211: Daphnia magna reproduction test, OECD guidelines for the testing of chemicals, section 2. OECD. doi: 10.1787/9789264185203-en
  60. Paul RJ, Mertenskötter A, Pinkhaus O, Pirow R, Gigengack U, Buchen I, Koch M, Horn W, Zeis B (2012) Seasonal and interannual changes in water temperature affect the genetic structure of a Daphnia assemblage (D. longispina complex) through genotype-specific thermal tolerances. Limnol Oceanogr 57:619–633. doi: 10.4319/lo.2012.57.2.0619 CrossRefGoogle Scholar
  61. Quinn G, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University, CambridgeCrossRefGoogle Scholar
  62. Rabiet M, Margoum C, Gouy V, Carluer N, Coquery M (2010) Assessing pesticide concentrations and fluxes in the stream of a small vineyard catchment-effect of sampling frequency. Environ Pollut 158:737–748. doi: 10.1016/j.envpol.2009.10.014 CrossRefGoogle Scholar
  63. R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna http://www.r-project.org/
  64. Ritz C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229. doi: 10.1002/etc.7 CrossRefGoogle Scholar
  65. Ritz C, Streibig JC (2005) Bioassay Analysis using R. J Stat Softw 12:1–22CrossRefGoogle Scholar
  66. Sancho E, Villarroel MJ, Andreu E, Ferrando MD (2009) Disturbances in energy metabolism of Daphnia magna after exposure to tebuconazole. Chemosphere 74:1171–1178. doi: 10.1016/j.chemosphere.2008.11.076 CrossRefGoogle Scholar
  67. Scherer C, Seeland A, Oehlmann J, 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. Aquat Toxicol 138–139:105–115. doi: 10.1016/j.aquatox.2013.04.014 CrossRefGoogle Scholar
  68. Seeland A, Oehlmann J, Müller R (2012) Aquatic ecotoxicity of the fungicide pyrimethanil: effect profile under optimal and thermal stress conditions. Environ Pollut 168:161–169. doi: 10.1016/j.envpol.2012.04.020 CrossRefGoogle Scholar
  69. Seeland A, Albrand J, Oehlmann J, Müller R (2013) Life stage-specific effects of the fungicide pyrimethanil and temperature on the snail Physella acuta (Draparnaud, 1805) disclose the pitfalls for the aquatic risk assessment under global climate change. Environ Pollut 174:1–9. doi: 10.1016/j.envpol.2012.10.020 CrossRefGoogle Scholar
  70. Stampfli NC, Knillmann S, Liess M, Beketov MA (2011) Environmental context determines community sensitivity of freshwater zooplankton to a pesticide. Aquat Toxicol 104:116–124. doi: 10.1016/j.aquatox.2011.04.004 CrossRefGoogle Scholar
  71. Stampfli NC, Knillmann S, Liess M, Noskov YA, Schäfer RB, Beketov MA (2013) Two stressors and a community: effects of hydrological disturbance and a toxicant on freshwater zooplankton. Aquat Toxicol 127:9–20. doi: 10.1016/j.aquatox.2012.09.003 CrossRefGoogle Scholar
  72. Tassou KT, Schulz R (2012) Combined effects of temperature and pyriproxyfen stress in a full life-cycle test with Chironomus riparius (Insecta). Environ Toxicol Chem 31:2384–2390. doi: 10.1002/etc.1969 CrossRefGoogle Scholar
  73. Van Doorslaer W, Stoks R, Jeppesen E, De Meester L (2007) Adaptive microevolutionary responses to simulated global warming in Simocephalus vetulus: a mesocosm study. Glob Chang Biol 13:878–886. doi: 10.1111/j.1365-2486.2007.01317.x CrossRefGoogle Scholar
  74. Van Doorslaer W, Stoks R, Duvivier C, Bednarska A, De Meester L (2009a) Population dynamics determine genetic adaptation to temperature in Daphnia. Evolution 63:1867–1878. doi: 10.1111/j.1558-5646.2009.00679.x CrossRefGoogle Scholar
  75. Van Doorslaer W, Vanoverbeke J, Duvivier C, Rousseaux S, Jansen M, Jansen B, Feuchtmayr H, Atkinson D, Moss B, Stoks R, De Meester L (2009b) Local adaptation to higher temperatures reduces immigration success of genotypes from a warmer region in the water flea Daphnia. Glob Chang Biol 15:3046–3055. doi: 10.1111/j.1365-2486.2009.01980.x CrossRefGoogle Scholar
  76. Van Doorslaer W, Stoks R, Swillen I, Feuchtmayr H, Atkinson D, Moss B, De Meester L (2010) Experimental thermal microevolution in community-embedded Daphnia populations. Clim Res 43:81–89. doi: 10.3354/cr00894 CrossRefGoogle Scholar
  77. Wilson RRS, Franklin CCE (2002) Testing the beneficial acclimation hypothesis. Trends Ecol Evol 17:66–70. doi: 10.1016/S0169-5347(01)02384-9 CrossRefGoogle Scholar
  78. Winder M, Schindler D (2004) Climate Change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106. doi: 10.1890/04-0151 CrossRefGoogle Scholar
  79. Wojtal-Frankiewicz A (2011) The effects of global warming on Daphnia spp. population dynamics: a review. Aquat Ecol 46:37–53. doi: 10.1007/s10452-011-9380-x CrossRefGoogle Scholar
  80. Yin M, Laforsch C, Lohr JN, Wolinska J (2011) Predator-induced defense makes Daphnia more vulnerable to parasites. Evolution 65:1482–1488. doi: 10.1111/j.1558-5646.2011.01240.x CrossRefGoogle Scholar
  81. Zeis B, Maurer J, Pinkhaus O, Bongartz E, Paul RJ (2004) A swimming activity assay shows that the thermal tolerance of Daphnia magna is influenced by temperature acclimation. Can J Zool 82:1605–1613. doi: 10.1139/z04-141 CrossRefGoogle Scholar
  82. Zhang L, Gibble R, Baer KN (2003) The effects of 4-nonylphenol and ethanol on acute toxicity, embryo development, and reproduction in Daphnia magna. Ecotoxicol Environ Saf 55:330–337. doi: 10.1016/S0147-6513(02)00081-7 CrossRefGoogle Scholar
  83. Zubrod JP, Bundschuh M, Schulz R (2010) Effects of subchronic fungicide exposure on the energy processing of Gammarus fossarum (Crustacea; Amphipoda). Ecotoxicol Environ Saf 73:1674–1680. doi: 10.1016/j.ecoenv.2010.07.046 CrossRefGoogle Scholar
  84. Zubrod JP, Baudy P, Schulz R, Bundschuh M (2014) Effects of current-use fungicides and their mixtures on the feeding and survival of the key shredder Gammarus fossarum. Aquat Toxicol 150:133–143. doi: 10.1016/j.aquatox.2014.03.002 CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of AveiroAveiroPortugal
  2. 2.CESAMUniversity of AveiroAveiroPortugal
  3. 3.Department of Environment and PlanningUniversity of AveiroAveiroPortugal
  4. 4.Department of Ecosystem ResearchLeibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB)BerlinGermany
  5. 5.Department of Biology, Chemistry, Pharmacy, Institute of BiologyFreie Universität BerlinBerlinGermany
  6. 6.CBMA (Centre of Molecular and Environmental Biology), Department of BiologyUniversity of MinhoBragaPortugal

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