Abstract
The origin of the populations used in ecotoxicological bioassays (from nature (wild populations) or from cultures (laboratory populations)) could have a key influence on the sensitivity of the tested species to different toxicants. However, the available information on this subject is scarce. To assess the likely influence of the population origin (wild vs. laboratory) of species–genus on the toxicant tolerance, we performed a quantitative review of the ECOTOX database, from which we collected the effective concentrations for a wide range of compounds (metals and organics), endpoints, and exposure times. We found a general trend of lower sensitivity of wild populations to toxicants than laboratory populations, although sensitivity was dependent on species and toxicant groups. This suggests that the results of bioassays with laboratory populations may overestimate the toxicity of most of the compounds. Our study highlights the relevance of the origin of the populations in the determination of the sensitivity of species to toxicants. This study also warns about the biases in the species and toxicants used in ecotoxicology, which may lead to an underrepresentation of the biodiversity and the toxicological context of aquatic ecosystems.
Similar content being viewed by others
Availability of data and materials
Raw data are publicly available in the Figshare online repository: https://doi.org/10.6084/m9.figshare.17040470.v2.
References
Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12. https://doi.org/10.2478/v10102-009-0001-7
Alonso A, Camargo JA (2003) Short-term toxicity of ammonia, nitrite, and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bull Environ Contam Toxicol 70:1006–1012. https://doi.org/10.1007/s00128-003-0082-5
Amiard-Triquet C, Cossu-Leguille C, Mouneyrac C (2012) Biomarkers of defense, tolerance, and ecological consequences. In: Amiard-Triquet C, Amiard JC, Rainbow PS (eds) Ecological biomarkers: indicators of ecotoxicological effects. CRC Press, Boca Raton, pp 45–72
Baird DJ, Van den Brink PJ (2007) Using biological traits to predict species sensitivity to toxic substances. Ecotoxicol Environ Saf 67:296–301. https://doi.org/10.1016/j.ecoenv.2006.07.001
Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol Part C Toxicol Pharmacol 140:175–186. https://doi.org/10.1016/j.cca.2005.01.013
Bray JP, Reich J, Nichols SJ, KonKam King G, Mac Nally R, Thompson R, Oreilly-Nugent A, Kefford BJ (2019) Biological interactions mediate context and species-specific sensitivities to salinity. Philos Trans R Soc B Biol Sci 374:20180020. https://doi.org/10.1098/rstb.2018.0020
Brouwer A, Murk AJ, Koeman JH (1990) Biochemical and physiological approaches in ecotoxicology. Funct Ecol 4:275. https://doi.org/10.2307/2389586
Brown AF, Pascoe D (1989) Parasitism and host sensitivity to cadmium: an acanthocephalan infection of the freshwater amphipod Gammarus pulex. J Appl Ecol 26:473. https://doi.org/10.2307/2404075
Brown AR, Hosken DJ, Balloux F, Bickley LK, LePage G, Owen SF, Hetheridge MJ, Tyler CR (2009) Genetic variation, inbreeding and chemical exposure—combined effects in wildlife and critical considerations for ecotoxicology. Philos Trans r Soc B Biol Sci 364:3377–3390. https://doi.org/10.1098/rstb.2009.0126
Brown AR, Bickley LK, Le Page G, Hosken DJ, Paull GC, Hamilton PB, Owen SF, Robinson J, Sharpe AD, Tyler CR (2011) Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations? − A case study with an endocrine disrupting chemical. Environ Sci Technol 45:4166–4172. https://doi.org/10.1021/es200122r
Chekroun KB, Baghour M (2013) The role of algae in phytoremediation of heavy metals: a review. J Mater Environ Sci 4:873–880
Correia AD, Costa MH, Luis OJ, Livingstone DR (2003) Age-related changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in whole body Gammarus locusta (Crustacea: Amphipoda). J Exp Mar Biol Ecol 289:83–101. https://doi.org/10.1016/S0022-0981(03)00040-6
Couture P, Pyle G (2008) Live fast and die young: metal effects on condition and physiology of wild yellow perch from along two metal contamination gradients. Hum Ecol Risk Assess 14:73–96. https://doi.org/10.1080/10807030701790322
Crane M, Burton GA, Culp JM, Greenberg MS, Munkittrick KR, Ribeiro R, Salazar MH, St-Jean SD (2007) Review of aquatic in situ approaches for stressor and effect diagnosis. Integr Environ Assess Manag 3:234. https://doi.org/10.1897/IEAM_2006-027.1
DelValls TA, Conradi M (2000) Advances in marine ecotoxicology: laboratory tests versus field assessment data on sediment quality studies. Cienc Mar 26:39–64. https://doi.org/10.7773/cm.v26i1.572
Dhir B, Sharmila P, Saradhi PP (2009) Potential of aquatic macrophytes for removing contaminants from the environment. Crit Rev Environ Sci Technol 39:754–781. https://doi.org/10.1080/10643380801977776
Ebele AJ, Abou-Elwafa Abdallah M, Harrad S (2017) Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3:1–16. https://doi.org/10.1016/j.emcon.2016.12.004
Fan W, Xu Z, Wang W-X (2015) Contrasting metal detoxification in polychaetes, bivalves and fish from a contaminated bay. Aquat Toxicol 159:62–68. https://doi.org/10.1016/j.aquatox.2014.11.024
Forni C, Tommasi F (2016) Duckweed: a tool for ecotoxicology and a candidate for phytoremediation. Curr Biotechnol 5:2–10. https://doi.org/10.2174/2211550104666150819190629
Gashkina NA, Moiseenko TI, Kudryavtseva LP (2020) Fish response of metal bioaccumulation to reduced toxic load on long-term contaminated lake Imandra. Ecotoxicol Environ Saf 191:110205. https://doi.org/10.1016/j.ecoenv.2020.110205
Gupta C, Prakash D (2013) Duckweed: an effective tool for phyto-remediation. Toxicol Environ Chem 95:1256–1266. https://doi.org/10.1080/02772248.2013.879309
Gustafson A-L, Stedman DB, Ball J, Hillegass HM, Flood A, Zhang CX, Panzica-Kelly J, Cao J, Coburn A, Enright BP, Tornesi MB, Hetheridge M, Augustine-Rauch KA (2012) Inter-laboratory assessment of a harmonized zebrafish developmental toxicology assay - Progress report on phase I. Reprod Toxicol 33(2):155–164. https://doi.org/10.1016/j.reprotox.2011.12.004
Häder D-P, Banaszak AT, Villafañe VE, Narvarte MA, González RA, Helbling EW (2020) Anthropogenic pollution of aquatic ecosystems: emerging problems with global implications. Sci Total Environ 713:136586. https://doi.org/10.1016/j.scitotenv.2020.136586
Hamilton PB, Cowx IG, Oleksiak MF, Griffiths AM, Grahn M, Stevens JR, Carvalho GR, Nicol E, Tyler CR (2015) Population-level consequences for wild fish exposed to sublethal concentrations of chemicals – a critical review. Fish Fish 17:545–566. https://doi.org/10.1111/faf.12125
Hodgson E (2004) A textbook of modern toxicology, 3rd edn. John Wiley, Hoboken
Hoy M, Boese BL, Taylor L, Reusser D, Rodriguez R (2012) Salinity adaptation of the invasive New Zealand mud snail (Potamopyrgus antipodarum) in the Columbia River estuary (Pacific Northwest, USA): physiological and molecular studies. Aquat Ecol 46:249–260. https://doi.org/10.1007/s10452-012-9396-x
Hylland K (2006) Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems. J Toxicol Environ Health A 69:109–123. https://doi.org/10.1080/15287390500259327
Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176. https://doi.org/10.1086/598822
Jesenska S, Nemethova S, Blaha L (2013) Validation of the species sensitivity distribution in retrospective risk assessment of herbicides at the river basin scale—the Scheldt river basin case study. Environ Sci Pollut Res 20:6070–6084. https://doi.org/10.1007/s11356-013-1644-7
Jordão R, Campos B, Lemos MFL, Soares AMVM, Tauler R, Barata C (2016) Induction of multixenobiotic defense mechanisms in resistant Daphnia magna clones as a general cellular response to stress. Aquat Toxicol 175:132–143. https://doi.org/10.1016/j.aquatox.2016.03.015
Kaonga CC, Kumwenda J, Mapoma HT (2010) Accumulation of lead, cadmium, manganese, copper and zinc by sludge worms; Tubifex tubifex in sewage sludge. Int J Environ Sci Technol 7:119–126. https://doi.org/10.1007/BF03326123
Khan AT, Weis JS, D’Andrea L (1988) Studies of cadmium tolerance in two populations of grass shrimp, Palaemonetes pugio. Bull Environ Contam Toxicol 40:30–34. https://doi.org/10.1007/BF01689382
Khan FR, Irving JR, Bury NR, Hogstrand C (2011) Differential tolerance of two Gammarus pulex populations transplanted from different metallogenic regions to a polymetal gradient. Aquat Toxicol 102:95–103. https://doi.org/10.1016/j.aquatox.2011.01.001
Kimball KD, Levin SA (1985) Limitations of laboratory bioassays: the need for ecosystem-level testing. Bioscience 35:165–171. https://doi.org/10.2307/1309866
Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205. https://doi.org/10.1016/0269-7491(87)90057-1
Lagrana CC, Apodaca DC, David CPC (2011) Chironomids as biological indicators of metal contamination in aquatic environment. Int J Environ Sci Dev 2:306–310
Leblanc GA (1982) Laboratory investigation into the development of resistance of Daphnia magna (Straus) to environmental pollutants. Environ Pollut Ser a Ecol Biol 27:309–322. https://doi.org/10.1016/0143-1471(82)90159-3
Major K, Soucek DJ, Giordano R, Wetzel MJ, Soto-Adames F (2013) The common ecotoxicology laboratory strain of Hyalella azteca is genetically distinct from most wild strains sampled in eastern North America: common lab strain of H. azteca is distinct from wild strains. Environ Toxicol Chem 32:2637–2647. https://doi.org/10.1002/etc.2355
Maltby L, Crane M (1994) Responses of Gammarus pulex (Amphipoda, Crustacea) to metalliferous effluents: identification of toxic components and the importance of interpopulation variation. Environ Pollut 84:45–52. https://doi.org/10.1016/0269-7491(94)90069-8
Maltby L, Blake N, Brock TCM, Van den Brink PJ (2005) Insecticide species sensitivity distributions: importance of test species selection and relevance to aquatic ecosystems. Environ Toxicol Chem 24:379. https://doi.org/10.1897/04-025R.1
Mamun AA, Amid A, Karim IA, Rashid SS (2012). Phytoremediation of partially treated wastewater by Chlorella vulgaris. International Conference on Chemical Processes and Environmental Issues, Singapore, 192–195.
Marie V, Baudrimont M, Boudou A (2006) Cadmium and zinc bioaccumulation and metallothionein response in two freshwater bivalves (Corbicula fluminea and Dreissena polymorpha) transplanted along a polymetallic gradient. Chemosphere 65:609–617. https://doi.org/10.1016/j.chemosphere.2006.01.074
Marshall JS (1978) Field verification of cadmium toxicity to laboratory Daphnia populations. Bull Environ Contam Toxicol 20:387–393. https://doi.org/10.1007/BF01683536
Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418–427. https://doi.org/10.1890/07-0449.1
Martín-Folgar R, Martínez-Guitarte J-L (2017) Cadmium alters the expression of small heat shock protein genes in the aquatic midge Chironomus riparius. Chemosphere 169:485–492. https://doi.org/10.1016/j.chemosphere.2016.11.067
Moreno Abril SI, Dalmolin C, Costa PG, Bianchini A (2018) Expression of genes related to metal metabolism in the freshwater fish Hyphessobrycon luetkenii living in a historically contaminated area associated with copper mining. Environ Toxicol Pharmacol 60:146–156. https://doi.org/10.1016/j.etap.2018.04.019
Newman MC (2015) Fundamentals of ecotoxicology, 4th edn. CRC Press, Boca Ratón
Nowak C, Vogt C, Diogo JB, Schwenk K (2007) Genetic impoverishment in laboratory cultures of the test organism Chironomus riparius. Environ Toxicol Chem 26:1018. https://doi.org/10.1897/06-349R.1
Olafson RW, Kearns A, Sim RG (1979) Heavy metal induction of metallothionein synthesis in the hepatopancreas of the crab Scylla serrata. Comp Biochem Physiol Part B Comp Biochem 62:417–424. https://doi.org/10.1016/0305-0491(79)90112-3
Pereira JL, Hill CJ, Sibly RM, Bolshakov VN, Gonçalves F, Heckmann L-H, Callaghan A (2010) Gene transcription in Daphnia magna: effects of acute exposure to a carbamate insecticide and an acetanilide herbicide. Aquat Toxicol 97:268–276. https://doi.org/10.1016/j.aquatox.2009.12.023
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Romero-Blanco A, Alonso Á (2019) Tolerance assessment of the aquatic invasive snail Potamopyrgus antipodarum to different post-dispersive conditions: implications for its invasive success. NeoBiota 44:57–73. https://doi.org/10.3897/neobiota.44.31840
Schipper CA, Dubbeldam M, Feist SW, Rietjens IMCM, Murk AT (2008) Cultivation of the heart urchin Echinocardium cordatum and validation of its use in marine toxicity testing for environmental risk assessment. J Exp Mar Biol Ecol 364:11–18. https://doi.org/10.1016/j.jembe.2008.06.014
Smol JP (2008) Pollution of lakes and rivers: a paleoenvironmental perspective, 2nd edn. Blackwell Publishing, Malden
Somparn A, Iwai CB, Noller B (2015) Potential use of acetylcholinesterase, glutathione-S-transferase and metallothionein for assessment of contaminated sediment in tropical chironomid, Chironomus javanus. J Environ Biol 36:1355–1359
Soucek DJ, Dickinson A, Major KM, McEwen AR (2013) Effect of test duration and feeding on relative sensitivity of genetically distinct clades of Hyalella azteca. Ecotoxicology 22:1359–1366. https://doi.org/10.1007/s10646-013-1122-5
Sroda S, Cossu-Leguille C (2011) Seasonal variability of antioxidant biomarkers and energy reserves in the freshwater gammarid Gammarus roeseli. Chemosphere 83:538–544. https://doi.org/10.1016/j.chemosphere.2010.12.023
Thorp JH, Gloss SP (1986) Field and laboratory tests on acute toxicity of cadmium to freshwater crayfish. Bull Environ Contam Toxicol 37:355–361. https://doi.org/10.1007/BF01607773
Toušová Z, Kuta J, Hynek D, Adam V, Kizek R, Bláha L, Hilscherová K (2016) Metallothionein modulation in relation to cadmium bioaccumulation and age-dependent sensitivity of Chironomus riparius larvae. Environ Sci Pollut Res 23:10504–10513. https://doi.org/10.1007/s11356-016-6362-5
Tsui MTK, Wang WX (2007) Biokinetics and tolerance development of toxic metals in Daphnia magna. Environ Toxicol Chem 26:1023. https://doi.org/10.1897/06-430R.1
United States Environmental Protection Agency (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms. U.S Environmental Protection Agency, Washington DC, p 335
United States Environmental Protection Agency (2019) User guide: ECOTOXicology Database System, version 5.2. U.S. Environmental Protection Agency, Washington DC, p 90
United States Environmental Protection Agency (2016). Basic information on PFAS. https://www.epa.gov/pfas/basic-information-pfas (Accessed June 2020)
Uren Webster TM, Bury N, van Aerle R, Santos EM (2013) Global transcriptome profiling reveals molecular mechanisms of metal tolerance in a chronically exposed wild population of brown trout. Environ Sci Technol 47:8869–8877. https://doi.org/10.1021/es401380p
Van de Perre D, Janssen CR, De Schamphelaere KAC (2018) Combined effects of interspecies interaction, temperature, and zinc on Daphnia longispina population dynamics: Zn, temperature, interspecies interaction on D. longispina dynamics. Environ Toxicol Chem 37:1668–1678. https://doi.org/10.1002/etc.4115
Van den Brink PJ, Blake N, Brock TCM, Maltby L (2006) Predictive value of species sensitivity distributions for effects of herbicides in freshwater ecosystems. Hum Ecol Risk Assess Int J 12:645–674. https://doi.org/10.1080/10807030500430559
van Straalen NM, Timmermans MJTN (2002) Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Hum Ecol Risk Assess Int J 8:983–1002. https://doi.org/10.1080/1080-700291905783
Vandegehuchte MB, De Coninck D, Vandenbrouck T, De Coen WM, Janssen CR (2010) Gene transcription profiles, global DNA methylation and potential transgenerational epigenetic effects related to Zn exposure history in Daphnia magna. Environ Pollut 158:3323–3329. https://doi.org/10.1016/j.envpol.2010.07.023
Viarengo A, Canesi L, Pertica M, Livingstone DR (1991) Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comp Biochem Physiol Part C Comp Pharmacol 100:187–190. https://doi.org/10.1016/0742-8413(91)90151-I
Victor KK, Séka Y, Norbert KK, Sanogo TA, Celestin AB (2016) Phytoremediation of wastewater toxicity using water hyacinth (Eichhornia crassipes) and water lettuce (Pistia stratiotes). Int J Phytoremediation 18:949–955. https://doi.org/10.1080/15226514.2016.1183567
Vigneron A, Geffard O, Coquery M, François A, Quéau H, Chaumot A (2015) Evolution of cadmium tolerance and associated costs in a Gammarus fossarum population inhabiting a low-level contaminated stream. Ecotoxicology 24:1239–1249. https://doi.org/10.1007/s10646-015-1491-z
Williams KA, Green DWJ, Pascoe D, Gower DE (1986) The acute toxicity of cadmium to different larval stages of Chironomus riparius (Diptera: Chironomidae) and its ecological significance for pollution regulation. Oecologia 70:362–366. https://doi.org/10.1007/BF00379498
Wogram J, Liess M (2001) Rank ordering of macroinvertebrate species sensitivity to toxic compounds by comparison with that of Daphnia magna. Bull Environ Contam Toxicol 67:360–367. https://doi.org/10.1007/s001280133
Wuerthner VP, Jaeger J, Garramone PS, Loomis CO, Pecheny Y, Reynolds R, Deluna L, Klein S, Lam M, Hua J, Meindl GA (2019) Inducible pesticide tolerance in Daphnia pulex influenced by resource availability. Eco Evol 9:1182–1190. https://doi.org/10.1002/ece3.4807
Xie L, Klerks PL (2003) Responses to selection for cadmium resistance in the least killifish, Heterandria formosa. Environ Toxicol Chem 22:313–320. https://doi.org/10.1002/etc.5620220211
Zhu Q, Yang Y, Zhong Y, Lao Z, O’Neill P, Hong D, Zhang K, Zhao S (2020) Synthesis, insecticidal activity, resistance, photodegradation and toxicity of pyrethroids (a review). Chemosphere 254:126779. https://doi.org/10.1016/j.chemosphere.2020.126779
Acknowledgements
We want to extend our gratitude to Daniel Antúnez for suggesting improvements for the English usage in this manuscript. Part of this work was carried out within the sabbatical period of A.A. as a full professor in the University of Alcalá for the 2021–2022 academic year.
Funding
This project was funded by Universidad de Alcalá (research projects CCG2013/EXP-054, CCG2016/EXP-054, and CCG2018/EXP-074), by the Ministerio de Economía, Industria y Competitividad of Spain (research projects INTERTOX RTI2018-096046-B-C21 (MCIU/AEI/FEDER, UE) and EXARBIN RTI2018-093504-B-I00 (MCIU/AEI/FEDER, UE)), and by the Youth Employment Initiative of the European Social Fund.
Author information
Authors and Affiliations
Contributions
A.R.-B.: conceptualization, formal analysis, investigation, methodology, writing—original draft, writing—review and editing, visualization. A.A.: conceptualization, methodology, writing—review and editing, supervision, project administration, funding acquisition.
Corresponding author
Additional information
Responsible Editor: Bruno Nunes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Romero-Blanco, A., Alonso, Á. Laboratory versus wild populations: the importance of population origin in aquatic ecotoxicology. Environ Sci Pollut Res 29, 22798–22808 (2022). https://doi.org/10.1007/s11356-021-17370-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-17370-0