Genotype diversity promotes the persistence of Daphnia populations exposed to severe copper stress.
Daphnia
adaptation
copper
extirpation
genetic diversity
persistence
pollution
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
revised:
15
12
2021
received:
16
05
2021
accepted:
20
12
2021
pubmed:
10
1
2022
medline:
9
3
2022
entrez:
9
1
2022
Statut:
ppublish
Résumé
When environmental stressors of high intensity are sustained for long periods of time, populations face high probabilities of being extirpated. However, depending on the intensity of the stressor, large populations with sufficient genetic diversity may persist. We report the results of an experiment that tracked the persistence of Daphnia populations exposed to copper contamination. We assessed whether genotypic diversity reduced the risk of extinction. We created monoclonal and multiclonal populations and monitored their population sizes during a 32-week experiment. Cu was applied at a sub-lethal concentration and then increased every week until the population sizes dropped to about 10% of the carrying capacity (Cu at 180 μg/L). The concentration was then increased up to 186 μg/L and held stable until the end of the experiment. A survival analysis showed that clonal diversity extended the persistence of Daphnia populations, but copper contamination caused a substantial genetic erosion followed by population extirpation. However, some Cu-treated populations, mostly multiclonal, showed U-shaped patterns of growth consistent with evolutionary rescue but these did not lead to lasting population recovery. These results highlight the importance of genetic variation for population persistence, but they also show how quickly it can be lost in contaminated environments.
Substances chimiques
Copper
789U1901C5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
265-277Informations de copyright
© 2022 European Society for Evolutionary Biology.
Références
Agashe, D., Falk, J. J., & Bolnick, D. I. (2011). Effects of founding genetic variation on adaptation to a novel resource. Evolution, 65, 2481-2491. https://doi.org/10.1111/j.1558-5646.2011.01307.x
Agra, A. R., Guilhermino, L., Soares, A. M., & Barata, C. (2010). Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environmental Toxicology and Chemistry, 29, 939-946.
Agra, A. R., Soares, A. M., & Barata, C. (2011). Life-history consequences of adaptation to pollution. “Daphnia longispina clones historically exposed to copper”. Ecotoxicology, 20, 552-562. https://doi.org/10.1007/s10646-011-0621-5
Altshuler, I., Demiri, B., Xu, S., Constantin, A., Yan, N. D., & Cristescu, M. E. (2011). An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integrative and Comparative Biology, 51, 623-633. https://doi.org/10.1093/icb/icr103
Armbruster, P., & Reed, D. H. (2005). Inbreeding depression in benign and stressful environments. Heredity, 95, 235-242. https://doi.org/10.1038/sj.hdy.6800721
Baird, D., Barber, I., & Calow, P. (1990). Clonal variation in general responses of Daphnia magna Straus to toxic stress. I. Chronic life-history effects. Functional Ecology, 4, 399-407.
Barnosky, A. D., Matzke, N., Tomiya, S., Wogan, G. O. U., Swartz, B., Quental, T. B., Marshall, C., McGuire, J. L., Lindsey, E. L., Maguire, K. C., Mersey, B., & Ferrer, E. A. (2011). Has the Earth's sixth mass extinction already arrived? Nature, 471, 51-57. https://doi.org/10.1038/nature09678
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48.
Bell, G. (2013). Evolutionary rescue and the limits of adaptation. Philosophical Transactions of the Royal Society B, 368, 20120080. https://doi.org/10.1098/rstb.2012.0080
Bell, G. (2017). Evolutionary rescue. Annual Review of Ecology, Evolution, and Systematics, 48(1), 605-627. https://doi.org/10.1146/annurev-ecolsys-110316-023011
Bickham, J. W., Sandhu, S., Hebert, P. D., Chikhi, L., & Athwal, R. (2000). Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutation Research/Reviews in Mutation Research, 463, 33-51. https://doi.org/10.1016/S1383-5742(00)00004-1
Bijlsma, R., & Loeschcke, V. (2012). Genetic erosion impedes adaptive responses to stressful environments. Evolutionary Applications, 5, 117-129. https://doi.org/10.1111/j.1752-4571.2011.00214.x
Bossuyt, B. T. A., Escobar, Y. R., & Janssen, C. R. (2005). Multigenerational acclimation of Daphnia magna straus to different bioavailable copper concentrations. Ecotoxicology and Environmental Safety, 61, 327-336.
Bradshaw, A. (1991). The Croonian Lecture, 1991: Genostasis and the limits to evolution. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 333, 289-305.
Brook, B. W., Sodhi, N. S., & Bradshaw, C. J. (2008). Synergies among extinction drivers under global change. Trends in Ecology and Evolution, 23, 453-460. https://doi.org/10.1016/j.tree.2008.03.011
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multi-model inference: A practical information-theoretic approach (2nd ed., p. 83). Springer-Verlag.
Cao, Y., Zhang, S., Wang, G., Li, T., Xu, X., Deng, O., Zhang, Y., & Pu, Y. (2017). Enhancing the soil heavy metals removal efficiency by adding HPMA and PBTCA along with plant washing agents. Journal of Hazardous Materials, 339, 33-42. https://doi.org/10.1016/j.jhazmat.2017.06.007
Carlson, S. M., Cunningham, C. J., & Westley, P. A. (2014). Evolutionary rescue in a changing world. Trends in Ecology and Evolution, 29, 521-530. https://doi.org/10.1016/j.tree.2014.06.005
Ceballos, G., Ehrlich, P. R., Barnosky, A. D., García, A., Pringle, R. M., & Palmer, T. M. (2015). Accelerated modern human-induced species losses: Entering the sixth mass extinction. Science Advances, 1, e1400253. https://doi.org/10.1126/sciadv.1400253
Celis-Salgado, M. P., Cairns, A., Kim, N., & Yan, N. D. (2008). The FLAMES medium: a new, soft-water culture and bioassay medium for Cladocera. Internationale Vereinigung Für Theoretische und Angewandte Limnologie: Verhandlungen, 30, 265-271. https://doi.org/10.1080/03680770.2008.11902123
Chain, F. J., Finlayson, S., Crease, T., & Cristescu, M. (2019). Variation in transcriptional responses to copper exposure across Daphnia pulex lineages. Aquatic Toxicology, 210, 85-97.
Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villarreal, G., Dickson, M., Grimwood, J., Schmutz, J., Myers, R. M., Schluter, D., & Kingsley, D. M. (2005). Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928-1933. https://doi.org/10.1126/science.1107239
Coors, A., Vanoverbeke, J., De Bie, T., & De Meester, L. (2009). Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquatic Toxicology, 95, 71-79. https://doi.org/10.1016/j.aquatox.2009.08.004
Cristescu, M. E., Colbourne, J. K., Radivojac, J., & Lynch, M. (2006). A microsatellite-based genetic linkage map of the waterflea, Daphnia pulex: On the prospect of crustacean genomics. Genomics, 88, 415-430. https://doi.org/10.1016/j.ygeno.2006.03.007
Davis, P., & Ozburn, G. W. (1969). The pH tolerance of Daphnia pulex (Leydig, emend., Richard). Canadian Journal of Zoology, 47, 1173.
De Meester, L., Vanoverbeke, J., De Gelas, K., Ortells, R., & Spaak, P. (2006). Genetic structure of cyclic parthenogenetic zooplankton populations-a conceptual framework. Archiv Für Hydrobiologie, 167, 217-244. https://doi.org/10.1127/0003-9136/2006/0167-0217
De Schamphelaere, K. A. C., Forrez, I., Dierckens, K., Sorgeloos, P., & Janssen, C. R. (2007). Chronic toxicity of dietary copper to Daphnia magna. Aquatic Toxicology, 81, 409-418. https://doi.org/10.1016/j.aquatox.2007.01.002
Duruibe, J. O., Ogwuegbu, M. O. C., & Egwurugwu, J. N. (2007). Heavy metal pollution and human biotoxic effects. International Journal of Physical Sciences, 2, 112-118.
Dutilleul, M., Bonzom, J.-M., Lecomte, C., Goussen, B., Daian, F., Galas, S., & Réale, D. (2014). Rapid evolutionary responses of life history traits to different experimentally-induced pollutions in Caenorhabditis elegans. BMC Evolutionary Biology, 14, 252. https://doi.org/10.1186/s12862-014-0252-6
Ekroth, A. K. E., Rafaluk-Mohr, C., & King, K. C. (2019). Host genetic diversity limits parasite success beyond agricultural systems: a meta-analysis. Proceedings of the Royal Society B: Biological Sciences, 286, 20191811.
Eschbach, E., & Schöning, S. (2013). Identification of high-resolution microsatellites without a priori knowledge of genotypes using a simple scoring approach. Methods in Ecology and Evolution, 4, 1076-1082.
Feder, J. L., Berlocher, S. H., Roethele, J. B., Dambroski, H., Smith, J. J., Perry, W. L., Gavrilovic, V., Filchak, K. E., Rull, J., & Aluja, M. (2003). Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Sciences of the United States of America, 100, 10314-10319. https://doi.org/10.1073/pnas.1730757100
Felsenstein, J. (1974). The evolutionary advantage of recombination. Genetics, 78, 737-756. https://doi.org/10.1093/genetics/78.2.737
Fisher, R. (1930). The theory of natural selection. Oxford University Press.
Gibson, A. K., & Nguyen, A. E. (2020). Does genetic diversity protect host populations from parasites? A meta-analysis across natural and agricultural systems. Evolution Letters, 5, 16-32. https://doi.org/10.1002/evl3.206
Gienapp, P., Teplitsky, C., Alho, J., Mills, J., & Merilä, J. (2008). Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology, 17, 167-178. https://doi.org/10.1111/j.1365-294X.2007.03413.x
Gledhill, M., Nimmo, M., Stephen, J. H., & Brown, M. T. (1997). The toxicity of copper(II) species to marine algae, with particular reference to macroalgae. Journal of Phycology, 33, 2-11. https://doi.org/10.1111/j.0022-3646.1997.00002.x
Gonzalez, A., Ronce, O., Ferriere, R., & Hochberg, M. E. (2013). Evolutionary rescue: An emerging focus at the intersection between ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20120404.
Hairston, N. G. Jr, Kearns, C. M., Perry Demma, L., & Effler, S. W. (2005). Species-specific Daphnia phenotypes: A history of industrial pollution and pelagic ecosystem response. Ecology, 86, 1669-1678. https://doi.org/10.1890/03-0784
Haldane, J. B. S. (1957). The cost of natural selection. Journal of Genetics, 55, 511-524. https://doi.org/10.1007/BF02984069
Heugens, E. H. W., Hendriks, A. J., Dekker, T., Straalen, N. M. V., & 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, 247-284. https://doi.org/10.1080/20014091111695
Hochmuth, J. D., De Meester, L., Pereira, C. M., Janssen, C. R., & De Schamphelaere, K. A. (2015). Rapid adaptation of a Daphnia magna population to metal stress is associated with heterozygote excess. Environmental Science and Technology, 49, 9298-9307.
Hoffmann, A. A., & Willi, Y. (2008). Detecting genetic responses to environmental change. Nature Reviews Genetics, 9, 421-432. https://doi.org/10.1038/nrg2339
Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal: Journal of Mathematical Methods in Biosciences, 50, 346-363. https://doi.org/10.1002/bimj.200810425
Hughes, A. R., Inouye, B. D., Johnson, M. T., Underwood, N., & Vellend, M. (2008). Ecological consequences of genetic diversity. Ecology Letters, 11, 609-623. https://doi.org/10.1111/j.1461-0248.2008.01179.x
Huston, M. A. (1997). Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia, 110, 449-460. https://doi.org/10.1007/s004420050180
Kaplan, E. L., & Meier, P. (1958). Nonparametric estimation from incomplete observations. Journal of the American Statistical Association, 53, 457-481. https://doi.org/10.1080/01621459.1958.10501452
Kim, H., Koedrith, P., & Seo, Y. (2015). Ecotoxicogenomic approaches for understanding molecular mechanisms of environmental chemical toxicity using aquatic invertebrate, Daphnia model organism. International Journal of Molecular Sciences, 16, 12261-12287. https://doi.org/10.3390/ijms160612261
Kim, S. J., Rodriguez-Lanetty, M., Suh, J. H., & Song, J. I. (2003). Emergent effects of heavy metal pollution at a population level: Littorina brevicula as a study case. Marine Pollution Bulletin, 46, 74-80.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1-26.
Lachapelle, J., & Bell, G. (2012). Evolutionary rescue of sexual and asexual populations in a deteriorating environment. Evolution, 66, 3508-3518. https://doi.org/10.1111/j.1558-5646.2012.01697.x
Lampert, W. (2006). Daphnia: model herbivore, predator and prey. Polish Journal of Ecology, 54, 607-620.
Laskowski, R., Radwan, J., Kuduk, K., Mendrok, M., & Kramarz, P. (2015). Population growth rate and genetic variability of small and large populations of Red flour beetle (Tribolium castaneum) following multigenerational exposure to copper. Ecotoxicology, 24, 1162-1170. https://doi.org/10.1007/s10646-015-1463-3
Lenth, R., Singmann, H., Love, J., Buerkner, P., & Herve, M. (2019). Package “Emmeans”: Estimated marginal means, aka least-squares means (pp. 1-67). The Comprehnsive R Archive Network.
Loaring, J. M., & Hebert, P. D. (1981). Ecological differences among clones of Daphnia pulex Leydig. Oecologia, 51, 162-168. https://doi.org/10.1007/BF00540595
Long, K. E., Van Genderen, E. J., & Klaine, S. J. (2004). The effects of low hardness and pH on copper toxicity to Daphnia magna. Environmental Toxicology and Chemistry: An International Journal, 23, 72-75. https://doi.org/10.1897/02-486
Lopes, I., Baird, D., & Ribeiro, R. (2004). Genetic determination of tolerance to lethal and sublethal copper concentrations in field populations of Daphnia longispina. Archives of Environmental Contamination and Toxicology, 46, 43-51. https://doi.org/10.1007/s00244-003-2143-5
Lopes, I., Baird, D. J., & Ribeiro, R. (2006). Genetic adaptation to metal stress by natural populations of Daphnia longispina. Ecotoxicology and Environmental Safety, 63, 275-285. https://doi.org/10.1016/j.ecoenv.2004.12.015
Loria, A., Cristescu, M. E., & Gonzalez, A. (2019). Mixed evidence for adaptation to environmental pollution. Evolutionary Applications, 12, 1259-1273. https://doi.org/10.1111/eva.12782
Markert, J. A., Champlin, D. M., Gutjahr-Gobell, R., Grear, J. S., Kuhn, A., McGreevy, T. J., Roth, A., Bagley, M. J., & Nacci, D. E. (2010). Population genetic diversity and fitness in multiple environments. BMC Evolutionary Biology, 10, 205. https://doi.org/10.1186/1471-2148-10-205
Medina, M., Morandi, B., & Correa, J. (2009). Copper effects in the copepod Tigriopus angulatus Lang, 1933: Natural broad tolerance allows maintenance of food webs in copper-enriched coastal areas. Marine and Freshwater Research, 59, 1061-1066. https://doi.org/10.1071/MF08122
Millette, K., Fussmann, G., & Cristescu, M. E. (2021). Rapid decay of intraspecific genetic diversity in clonal assemblages. In K. L. Millette (Ed.), Human effects on intraspecific genetic diversity. (Vol. 2, pp. 16-56). McGill University, Ph.D. thesis.
Morgan, A. J., Kille, P., & Stürzenbaum, S. R. (2007). Microevolution and ecotoxicology of metals in invertebrates. Environmental Science and Technology, 41, 1085-1096. https://doi.org/10.1021/es061992x
Muyssen, B. T., Janssen, C. R., & Bossuyt, B. T. (2002). Tolerance and acclimation to zinc of field-collected Daphnia magna populations. Aquatic Toxicology, 56, 69-79. https://doi.org/10.1016/S0166-445X(01)00206-5
Nadig, S. G., Lee, K. L., & Adams, S. M. (1998). Evaluating alterations of genetic diversity in sunfish populations exposed to contaminants using RAPD assay. Aquatic Toxicology, 43, 163-178. https://doi.org/10.1016/S0166-445X(98)00049-6
Nriagu, J. O. (1996). A history of global metal pollution. Science, 272(5259), 223. https://doi.org/10.1126/science.272.5259.223
Osborne, R. K., Gillis, P. L., & Prosser, R. S. (2020). Transgenerational effects of copper on a freshwater gastropod, Planorbella Pilsbryi. Freshwater Mollusk Availability Biology and Conservation, 23, 42-54. https://doi.org/10.31931/fmbc.v22i2.2020.42-54
Oziolor, E. M., Reid, N. M., Yair, S., Lee, K. M., Guberman VerPloeg, S., Bruns, P. C., Shaw, J. R., Whitehead, A., & Matson, C. W. (2019). Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science, 364, 455-457. https://doi.org/10.1126/science.aav4155
Pelz, H.-J., Rost, S., Hünerberg, M., Fregin, A., Heiberg, A.-C., Baert, K., MacNicoll, A. D., Prescott, C. V., Walker, A.-S., Oldenburg, J., & Müller, C. R. (2005). The genetic basis of resistance to anticoagulants in rodents. Genetics, 170, 1839-1847. https://doi.org/10.1534/genetics.104.040360
Poynton, H. C., Varshavsky, J. R., Chang, B., Cavigiolio, G., Chan, S., Holman, P. S., Loguinov, A. V., Bauer, D. J., Komachi, K., Theil, E. C., Perkins, E. J., Hughes, O., & Perkins, E. J. (2007). Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environmental Science & Technology, 41, 1044-1050.
R Core Team. (2019). R: A language and environment for statistical computing, version 3.3. 1. R Foundation for Statistical Computing.
Ramsayer, J., Kaltz, O., & Hochberg, M. E. (2013). Evolutionary rescue in populations of Pseudomonas fluorescens across an antibiotic gradient. Evolutionary Applications, 6, 608-616.
Ribeiro, R., Baird, D. J., Soares, A. M., & Lopes, I. (2012). Contaminant driven genetic erosion: a case study with Daphnia longispina. Environmental Toxicology and Chemistry, 31, 977-982. https://doi.org/10.1002/etc.1802
Robinson, J. D., Wares, J. P., & Drake, J. M. (2013). Extinction hazards in experimental Daphnia magna populations: Effects of genotype diversity and environmental variation. Ecology and Evolution, 3, 233-243.
Sarma, S., & Nandini, S. (2006). Review of recent ecotoxicological studies on cladocerans. Journal of Environmental Science and Health Part B, 41, 1417-1430. https://doi.org/10.1080/03601230600964316
Saro, L., Lopes, I., Martins, N., & Ribeiro, R. (2012). Testing hypotheses on the resistance to metals by Daphnia longispina: differential acclimation, endpoints association, and fitness costs. Environmental Toxicology and Chemistry, 31, 909-915. https://doi.org/10.1002/etc.1762
Sasvari, A., Aguilar, L., Khan, M., & Schmitt, F. (2010). Guidelines for mainstreaming gender into national biodiversity strategies and action plans (pp. viii + 97). IUCN.
Steiner, C. C., Weber, J. N., & Hoekstra, H. E. (2007). Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biology, 5, e219. https://doi.org/10.1371/journal.pbio.0050219
Stoddard, J. L., & Harper, R. (2007). Effects of multi-generational exposure of Daphnia Magna to copper. Huxley College of the Environment, Western Washington University.
Suresh, S. (2019). Differential gene expression and splicing in distinct Daphnia pulex lineages under acute copper toxicity. University of Massachusetts Lowell.
Therneau, T. (2015). A package for survival analysis in S. version 2.38.
Thielsch, A., Brede, N., Petrusek, A., De Meester, L., & Schwenk, K. (2009). Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia. Molecular Ecology, 18, 1616-1628.
Tilman, D., Clark, M., Williams, D. R., Kimmel, K., Polasky, S., & Packer, C. (2017). Future threats to biodiversity and pathways to their prevention. Nature, 546, 73-81. https://doi.org/10.1038/nature22900
Tilman, D., Lehman, C. L., & Thomson, K. T. (1997). Plant diversity and ecosystem productivity: Theoretical considerations. Proceedings of the National Academy of Science of the United States of America, 94, 1857-1861. https://doi.org/10.1073/pnas.94.5.1857
Tomasiks, P., & Warren, D. M. (1996). The use of Daphnia in studies of metal pollution of aquatic systems. Environmental Reviews, 4, 25-64.
van Straalen, N. M., & Timmermans, M. J. (2002). Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Human and Ecological Risk Assessment, 8, 983-1002. https://doi.org/10.1080/1080-700291905783
Vander Wal, E., Garant, D., Festa-Bianchet, M., & Pelletier, F. (2013). Evolutionary rescue in vertebrates: Evidence, applications and uncertainty. Philosophical Transactions of the Royal Society B, 368, 20120090.
Vanoverbeke, J., De Gelas, K., & De Meester, L. (2007). Habitat size and the genetic structure of a cyclical parthenogen, Daphnia Magna. Heredity, 98, 419. https://doi.org/10.1038/sj.hdy.6800958
Vanoverbeke, J., & De Meester, L. (2010). Clonal erosion and genetic drift in cyclical parthenogens-The interplay between neutral and selective processes. Journal of Evolutionary Biology, 23, 997-1012. https://doi.org/10.1111/j.1420-9101.2010.01970.x
Vinebrooke, R. D., Cottingham, K. L., Norberg, J. Scheffer, M., Dodson, S. I., Maberly, S. C., & Sommer, U. (2004). Impacts of multiple stressors on biodiversity and ecosystem functioning: The role of species co-tolerance. Oikos, 104, 451-457. https://doi.org/10.1111/j.0030-1299.2004.13255.x
Venâncio, C., Ribeiro, R., Soares, A. M. V. M., & Lopes, I. (2021). Survival recovery rates by six clonal lineages of Daphnia longispina after intermittent exposures to copper. Chemosphere, 264, 128403. https://doi.org/10.1016/j.chemosphere.2020.128403
Ward, T. J., & Robinson, W. E. (2005). Evolution of cadmium resistance in Daphnia magna. Environmental Toxicology and Chemistry, 24, 2341-2349. https://doi.org/10.1897/04-429R.1
Waxman, D., & Peck, J. R. (1999). Sex and adaptation in a changing environment. Genetics, 153, 1041-1053. https://doi.org/10.1093/genetics/153.2.1041
Yan, N. D., Girard, R., Heneberry, J. H., Keller, W. B., Gunn, J. M., & Dillon, P. J. (2004). Recovery of copepod, but not cladoceran, zooplankton from severe and chronic effects of multiple stressors. Ecology Letters, 7, 452-460. https://doi.org/10.1111/j.1461-0248.2004.00599.x
Yan, N. D., Keller, W., Somers, K. M., Pawson, T. W., & Girard, R. E. (1996). Recovery of crustacean zooplankton communities from acid and metal contamination: comparing manipulated and reference lakes. Canadian Journal of Fisheries and Aquatic Sciences, 53, 1301-1327. https://doi.org/10.1139/f96-065
Zhu, B., Liu, L., Li, D. L., Ling, F., & Wang, G. X. (2014). Developmental toxicity in rare minnow (Gobiocypris rarus) embryos exposed to Cu, Zn and Cd. Ecotoxicology and Environmental Safety, 104, 269-227.