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Effects of thermal evolution on the stoichiometric responses to nano-ZnO under warming are not general: insights from experimental evolution

Abstract

A key challenge for ecological risk assessment of contaminants under global warming is to predict effects at higher levels of biological organisation. One approach to reach this goal is to study how contaminants and warming cause changes in body stoichiometry as these may potentially cascade through food webs. Furthermore, though contaminants typically interact with warming, how rapid adaptation to higher temperatures affects these interactions is poorly studied. Here, we examined the effects of an important contaminant (ZnO nanoparticles, nZnO) and mild warming (4 °C) on body stoichiometry (C, N, P and their ratios) of an aquatic keystone species, the water flea Daphnia magna. To evaluate whether thermal evolution impacts the effects of nZnO at higher temperatures, we compared two sets of clones from a thermal selection experiment where Daphnia were kept in outdoor mesocosms at ambient or ambient +4 °C temperatures for 2 years. Exposure to nZnO decreased key body stoichiometric ratios (C:N, C:P and a trend for N:P) while warming increased the body C:N ratio. The stoichiometric changes to nZnO and warming were mostly independent and could be partly explained by changes in the macromolecules sugars and fat. Exposure to nZnO decreased C-rich sugars contributing to a reduced %C. Warming reduced body %C due to decreased C-rich sugars and fat levels, yet warming decreased body N% even more resulting in a higher C:N ratio. The stoichiometric responses to nZnO at the higher temperature did not differ between the two sets of clones, indicating experimental thermal evolution did not change the effects of nZnO under warming. Studying the stoichiometric responses to nZnO and warming of this keystone species may provide novel insights on the toxic effects of contaminants under warming. Moreover, understanding the influence of thermal evolution on the toxicity of contaminants is important for ecological risk assessment especially in a warming world.

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References

  1. Adam N, Schmitt C, Galceran J et al. (2014) The chronic toxicity of ZnO nanoparticles and ZnCl2 to Daphnia magna and the use of different methods to assess nanoparticle aggregation and dissolution. Nanotoxicology 8:709–717

  2. Bacchetta R, Maran B, Marelli M et al. (2016) Role of soluble zinc in ZnO nanoparticle cytotoxicity in Daphnia magna: a morphological approach. Environ Res 148:376–385

  3. Bacchetta R, Santo N, Marelli M et al. (2017) Chronic toxicity effects of ZnSO4 and ZnO nanoparticles in Daphnia magna. Environ Res 152:128–140

  4. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R Packag version 1:1–23

  5. Beketov MA, Kefford BJ, Schäfer RB, Liess M (2013) Pesticides reduce regional biodiversity of stream invertebrates. Proc Natl Acad Sci USA 110:11039–11043

  6. Boxall AB, Tiede K, Chaudhry Q (2007) Engineered nanomaterials in soils and water: how do they behave and could they pose a risk to human health? Nanomedicine 2:919–927

  7. Dinh Van K, Janssens L, Debecker S et al. (2013) Susceptibility to a metal under global warming is shaped by thermal adaptation along a latitudinal gradient. Glob Change Biol 19:2625–2633

  8. Duffy JE, Cardinale BJ, France KE et al. (2007) The functional role of biodiversity in ecosystems: Incorporating trophic complexity. Ecol Lett 10:522–538

  9. Ek C, Karlson AML, Hansson S et al. (2015) Stable isotope composition in daphnia is modulated by growth, temperature, and toxic exposure: Implications for trophic magnification factor assessment. Environ Sci Technol 49:6934–6942

  10. Feuchtmayr H, Moran R, Hatton K et al. (2009) Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. J Appl Ecol 46:713–723

  11. Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27

  12. Fox J, Weisberg S (2011) An R companion to applied regression. Sage Publications

  13. Franks SJ, Hamann E, Weis AE (2018) Using the resurrection approach to understand contemporary evolution in changing environments. Evol Appl 11:17–28

  14. Geerts AN, Vanoverbeke J, Vanschoenwinkel B et al. (2015) Rapid evolution of thermal tolerance in the water flea Daphnia. Nat Clim Change 5:665–668

  15. Goitom E, Kilsdonk LJ, Brans K et al. (2018) Rapid evolution leads to differential population dynamics and top-down control in resurrected Daphnia populations. Evol Appl 11:96–111

  16. Hawlena D, Schmitz OJ (2010a) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556

  17. Hawlena D, Schmitz OJ (2010b) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci 107:15503–15507

  18. Hawlena D, Strickland MS, Bradford MA, Schmitz OJ (2012) Fear of predation slows plant-litter decomposition. Science 336:1434–1438

  19. Holmstrup M, Bindesbøl AM, Oostingh GJ et al. (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762

  20. Hua J, Wuerthner VP, Jones DK et al. (2017) Evolved pesticide tolerance influences susceptibility to parasites in amphibians. Evol Appl 10:802–812

  21. IPCC (2013) Climate Change 2013: The Physical Science Basis. Cambridge University Press, Cambridge, UK

  22. Jansen M, Coors A, Stoks R, De Meester L (2011a) Evolutionary ecotoxicology of pesticide resistance: a case study in Daphnia. Ecotoxicology 20:543–551

  23. Jansen M, Stoks R, Coors A et al. (2011) Collateral damage: rapid exposure-induced evolution of pesticide resistance leads to increased susceptibility to parasites. Evolution 65:2681–2691

  24. Janssens L, Op De Beeck L, Stoks R (2017) Stoichiometric responses to an agricultural pesticide are modified by predator cues. Environ Sci Technol 51:581–588

  25. Klingshirn CF (2007) ZnO: material, physics and applications. ChemPhysChem 8:782–803

  26. Lenormand T, Nougué O, Jabbour-Zahab R et al. (2018) Resurrection ecology in Artemia. Evol Appl 11:76–87

  27. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33

  28. Liess M, Foit K, Knillmann S et al. (2016) Predicting the synergy of multiple stress effects. Sci Rep. 6:32965

  29. Malaj E, von der Ohe PC, Grote M et al. (2014) Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. Proc Natl Acad Sci USA 111:9549–9554

  30. Mcfeeters BJ, Frost PC (2011) Temperature and the effects of elemental food quality on Daphnia. Freshw Biol 56:1447–1455

  31. Mcmahon TA, Halstead NT, Johnson S et al. (2012) Fungicide-induced declines of freshwater biodiversity modify ecosystem functions and services. Ecol Lett 15:714–722

  32. Met Office (2012) Historic Station Data in 2012. https://www.metoffice.gov.uk/public/weather/climate-historic/#?tab=climateHistoric

  33. Moe SJ, De Schamphelaere K, Clements WH et al. (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61

  34. Mos B, Kaposi KL, Rose AL et al. (2017) Moderate ocean warming mitigates, but more extreme warming exacerbates the impacts of zinc from engineered nanoparticles on a marine larva. Environ Pollut 228:190–200

  35. Muyssen BTA, Janssen CR, Bossuyt BTA (2002) Tolerance and acclimation to zinc of field-collected Daphnia magna populations. Aquat Toxicol 56:69–79

  36. Noyes PD, Lema SC (2015) Forecasting the impacts of chemical pollution and climate change interactions on the health of wildlife. Curr Zool 61:669–689

  37. OECD (2004) OECD Guideline for Testing of Chemicals (Daphnia sp., Acute Immobilisation Test)

  38. Orsini L, Spanier KI, De Meester L (2012) Genomic signature of natural and anthropogenic stress in wild populations of the waterflea Daphnia magna: validation in space, time and experimental evolution. Mol Ecol 21:2160–2175

  39. Peters K, Bundschuh M, Schäfer RB (2013) Review on the effects of toxicants on freshwater ecosystem functions. Environ Pollut 180:324–329

  40. Plum C, Hüsener M, Hillebrand H (2015) Multiple vs. single phytoplankton species alter stoichiometry of trophic interaction with zooplankton. Ecology 96:3075–3089

  41. R Core Team (2013) R: A language and environment for statistical computing.R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  42. Read DS, Matzke M, Gweon HS et al. (2016) Soil pH effects on the interactions between dissolved zinc, non-nano-and nano-ZnO with soil bacterial communities. Environ Sci Pollut Res 23:4120–4128

  43. Schmitz OJ (2013) Global climate change and the evolutionary ecology of ecosystem functioning. Ann N Y Acad Sci 1297:61–72

  44. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press

  45. Stoks R, Block MDe, Mcpeek MA (2006) Physiological costs of compensatory growth in a Damselfly. Ecology 87:1566–1574

  46. Stoks R, Geerts AN, De Meester L (2014) Evolutionary and plastic responses of freshwater invertebrates to climate change: realized patterns and future potential. Evol Appl 7:42–55

  47. Stoks R, Govaert L, Pauwels K et al. (2016) Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna. Ecol Lett 19:180–190

  48. Van Straalen NM (2003) Peer reviewed: ecotoxicology becomes stress ecology. Environ Sci Technol 37:324A–330A

  49. Vrede T, Persson J, Aronsen G (2002) The influence of food quality (P: C ratio) on RNA: DNA ratio and somatic growth rate of Daphnia. Limnol Oceanogr 47:487–494

  50. Wong SWY, Leung KMY (2014) Temperature-dependent toxicities of nano zinc oxide to marine diatom, amphipod and fish in relation to its aggregation size and ion dissolution. Nanotoxicology 8(Suppl 1):24–35

  51. Zhang C, Jansen M, De Meester L, Stoks R (2016) Energy storage and fecundity explain deviations from ecological stoichiometry predictions under global warming and size-selective predation. J Anim Ecol 85:1431–1441

  52. Zhang C, Jansen M, De Meester L, Stoks R (2019) Rapid evolution in response to warming does not affect the toxicity of a pollutant: Insights from experimental evolution in heated mesocosms. Evol Appl. https://doi.org/10.1111/eva.12772

  53. Zhang C, Jansen M, Smolders E et al. (2018) Stoichiometric responses to nano ZnO under warming are modified by thermal evolution in Daphnia magna. Aquat Toxicol 202:90–96

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Acknowledgements

Financial support came from China Postdoctoral Science Foundation (2019M662337), Research Grants from FWO Flanders (G.0943.15), the KU Leuven Research Fund (C16/17/002), and the Fundamental Research Funds of Shandong University (61460079614088).

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Correspondence to Chao Zhang.

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Zhang, C., De Meester, L. & Stoks, R. Effects of thermal evolution on the stoichiometric responses to nano-ZnO under warming are not general: insights from experimental evolution. Ecotoxicology (2020). https://doi.org/10.1007/s10646-020-02165-9

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Keywords

  • Body stoichiometry
  • Daphnia magna
  • Experimental thermal selection
  • Warming
  • Nano zinc oxide