https://doi.org/10.4081/jlimnol.2021.2015
Behavioural responses of juvenile Daphnia magna to two organophosphorus insecticides
Submitted: 18 March 2021
Accepted: 13 September 2021
Published: 7 October 2021
Accepted: 13 September 2021
Abstract Views: 2252
PDF: 317
Supplementary: 198
HTML: 143
Supplementary: 198
HTML: 143
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
In this study, the behaviour of Daphnia magna was studied under equipotent and sub-lethal concentrations of two pesticides congeners: chlorpyrifos (CPF; 5 ng L-1 to 50 ng L-1) and chlorpyrifos-methyl (CPF-m; 30 ng L-1 to 300 ng L-1) with aims to assess and compare the behavioural swimming responses (BSRs) of the cladocerans elicited by both compounds at different concentrations and exposure times. A video tracking analysis after 24 h and 48 h of exposure allowed us to evaluate different behavioural responses (distance moved, average velocity, active time, and average acceleration). The results indicate that BSRs are sensitive indicators of sub-lethal stress. Highly concentration- and time-response changes for both compounds were observed during the experiments. In particular, in the first 24 h of exposure, both compounds elicited a similar decreasing trend in swimming behaviour, in which CPF induced the highest decline. Further, hypoactivity was associated with the narcotic effects of both compounds. Conversely, after 48 h of exposure, we observed an increasing tendency in the swimming parameters, particularly at the highest tested concentrations. However, the compounds did not exhibit the same trend. Rather, CPF-m induced high variations from the control groups. This reversal trend could be due to the activation of compensatory mechanisms, such as feeding, searching, or avoidance behaviours. These results suggest that BSRs are measurable active responses of organisms, which are controlled by time.
Affum AO, Acquaah SO, Osae SD, Kwaansa-Ansah EE, 2018. Distribution and risk assessment of banned and other current-use pesticides in surface and groundwaters consumed in an agricultural catchment dominated by cocoa crops in the Ankobra Basin, Ghana. Sci. Total Environ. 633:630-640.
DOI: https://doi.org/10.1016/j.scitotenv.2018.03.129
Ägerstrand M, Kathryn A, Balshine S, Brodin T, Brooks BW, Maack G, McCallum ES, Pyle G, Saaristo M, Ford AT, 2020. Emerging investigator series: use of behavioural endpoints in the regulation of chemicals. Environ. Sci. Proc. Imp. 22:49.
DOI: https://doi.org/10.1039/C9EM00463G
Amiard-Triquet C, 2009. Behavioral disturbances: the missing link between suborganismal and supra-organismal responses to stress? Prospects based on Aquatic Research. Hum. Ecol. Risk. Assess. 15:87-110.
DOI: https://doi.org/10.1080/10807030802615543
Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrrano JA, Tietge JE, Villeneuve DL, 2010. Adverse Outcome Pathways: A Conceptual Framework To Support Ecotoxicology Research And Risk Assessment. Environ. Toxicol. Chem. 29:730–741.
DOI: https://doi.org/10.1002/etc.34
Baird D.J., Barata C, 1998. Variability in the response of daphnia clones to toxic substances: Are safety margins being compromised? In: J.P. Seiler, J.L. Autrup and H. Autrup (eds.), Diversification in Toxicology - Man and Environment. Archives of Toxicology. Springer.
DOI: https://doi.org/10.1007/978-3-642-46856-8_35
Bownik A, Jasieczek M, Kosztowny E, 2020. Ketoprofen affects swimming behavior and impairs physiological endpoints of Daphnia magna. Sci. Total. Environ. 725:138312.
DOI: https://doi.org/10.1016/j.scitotenv.2020.138312
Cairns J, Gruber D, 1980. A comparison of methods and instrumentation of biological early warning systems. Water. Resour. Bull. 16:261-266.
DOI: https://doi.org/10.1111/j.1752-1688.1980.tb02388.x
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S, 2012. Biodiversity loss and its impact on humanity. Nature 486:59-67.
DOI: https://doi.org/10.1038/nature11148
Ccanccapa A, Masiá A, Navarro-Ortega A, Picó Y, Barceló D, 2016. Pesticides in the Ebro River basin: occurrence and risk assessment. Environ. Pollut. 211:414-424,
DOI: https://doi.org/10.1016/j.envpol.2015.12.059
Chevalier J, Grote M, Keller M, Pandard P, Cachot J, 2014. A new multi-cell exposure system for continuous tracking of Daphnia behaviour for toxicity assessment. J. Environ. Anal. Toxicol. 5:246.
Chevalier J, Harscoët E, Keller M, Pandard P, Cachot J, Grotey M, 2015. Exploration of Daphnia behavioral effect profiles induced by a broad range of toxicants with different modes of action. Environ. Toxicol. Chem. 34:1760–1769.
DOI: https://doi.org/10.1002/etc.2979
Christensen T, Torben B, Lauridsen TL, Ravn HW, Bayley M, 2005. A comparison of feeding efficiency and swimming ability of Daphnia magna exposed to cypermethrin. Aquat. Toxicol. 73:210-220.
DOI: https://doi.org/10.1016/j.aquatox.2005.03.011
Christopher MT, David JS, Matthew JW, 2001. Fluorinated phosphorus compounds: Part 4. A lack of anticholinesterase activity for four tris (fluoroalkyl) phosphates. J. Fluorine Chem. 107:155-158.
DOI: https://doi.org/10.1016/S0022-1139(00)00394-8
De Souza RM, Seibert D, Quesada HB, de Jesus Bassetti F, Fagundes-Klen MR, Bergamasco R, 2020. Occurrence, impacts and general aspects of pesticides in surfacewater: A review. Process Saf. Environ. 135:22–37.
DOI: https://doi.org/10.1016/j.psep.2019.12.035
Dell’Omo G, 2002. Behavioural ecotoxicology. John Wiley & Sons, Chichester.
Di Nica V, González ABM, Lencioni V, Villa S, 2020. Behavioural and biochemical alterations by chlorpyrifos in aquatic insects: an emerging environmental concern for pristine Alpine habitats. Environ. Sci. Pollut. Res. 1-9.
Duquesne S, Küster E, 2010. Biochemical, metabolic, and behavioural responses and recovery of Daphnia magna after exposure to an organophosphate. Ecotox. and Environ. Saf., 73, 353-359.
DOI: https://doi.org/10.1016/j.ecoenv.2009.11.008
Ferrão‐Filho AS, Soares MCS, Lima RS, Magalhães VF, 2014. Effects of Cylindrospermopsis raciborskii (cyanobacteria) on the swimming behavior of Daphnia (cladocera). Environ. Toxicol. Chem. 33:223–229.
DOI: https://doi.org/10.1002/etc.2420
Ferrario C, Finizio A, Villa S, 2017. Legacy and emerging contaminants in meltwater of three Alpine glaciers. Sci. Total. Environ. 574:350e357.
DOI: https://doi.org/10.1016/j.scitotenv.2016.09.067
Ferrario C, Parolini M, De Felice B, Villa S, Finizio A, 2018. Linking sub-individual and supra-individual effects in Daphnia magna exposed to sub-lethal concentration of chlorpyrifos. Env. Poll. 235:411-418.
DOI: https://doi.org/10.1016/j.envpol.2017.12.113
Frey DG, 1982. Contrasting strategies of gamogenesis in Northern and Southern populations of Cladocera. Ecology. 63:223e241.
DOI: https://doi.org/10.2307/1937046
Fukuto, T.R., 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environ. Health Perspect. 87:245-254.
DOI: https://doi.org/10.1289/ehp.9087245
Gerhardt A, Carlsson A, Ressemann C, Stich KP, 1998. New online biomonitoring system for Gammarus pulex (L) (Crustacea): In situ test below a copper effluent in South Sweden. Environ. Sci. Technol. 32:150-156.
DOI: https://doi.org/10.1021/es970442j
Gerhardt A, 1999. Biomonitoring of polluted water. Reviews on Actual Topics. Environmental Research Forum 9. Trans.Tech. Publishers, Zürich.
DOI: https://doi.org/10.4028/www.scientific.net/RC.40
Gerhardt A, Janssens de Bisthoven, L, Soares AM, 2005. Evidence for the Stepwise Stress Model: Gambusia holbrooki and Daphnia magna under acid mine drainage and acidified reference water stress. Environ. Sci. Technol. 39:4150–4158.
DOI: https://doi.org/10.1021/es048589f
Hansen LR, Roslev P, 2016. Behavioural responses of juvenile Daphnia magna after exposure to glyphosate and glyphosate-copper complexes. Aquat. Toxicol. 179:36-43.
DOI: https://doi.org/10.1016/j.aquatox.2016.08.010
Hellou J, 2011. Behavioural ecotoxicology, an “early warning” signal to assess environmental quality. Environ. Sci. Pollut. Res. 18:1–11.
DOI: https://doi.org/10.1007/s11356-010-0367-2
Larsson P, and Kleiven OT, 1996. Food search and swimming speed in Daphnia, p. 375-387. In P.H. Lenz, D.K. Hartline, J.E. Purcell and D.L. Macmillan (eds.), Zooplankton: Sensory Ecology and Physiology. Gordon and Breach, Amsterdam.
DOI: https://doi.org/10.1201/9780203733615-28
Malaj E, von der Ohe PC, Grote M, Keuhne R, Mondy CP, Usseglio-Polatera P, Brack W, Scheafer RB, 2014. Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. P. Natl. Acad. Sci. USA 111:9549–9554.
DOI: https://doi.org/10.1073/pnas.1321082111
Melvin SD, Wilson SP, 2013. The utility of behavioral studies for aquatic toxicology testing: a meta-analysis. Chemosphere 93:2217-2223.
DOI: https://doi.org/10.1016/j.chemosphere.2013.07.036
Morselli M, Vitale CM, Ippolito A, Villa S, Giacchini R, Vighi M, Di Guardo A, 2018. Predicting pesticide fate in small cultivated mountain watersheds using the DynAPlus model: Toward improved assessment of peak exposure. Sci. Total Environ. 615:307-318.
DOI: https://doi.org/10.1016/j.scitotenv.2017.09.287
OECD, 2004. Guidelines for the testing of chemicals. Daphnia sp., Acute immobilisation test. OECD, Paris. Available from: https://www.oecd-ilibrary.org/docserver/9789264069947-en.pdf?expires=1633612307&id=id&accname=guest&checksum=B0EBF2FC18AD1F0EDC52AA6CACD0BE45
OECD, 2006. Test No. 201: Freshwater alga and cyanobacteria, growth inhibition test. OECD, Paris. Available from: https://search.oecd.org/env/test-no-201-alga-growth-inhibition-test-9789264069923-en.htm
OECD, 2019. Guidance document on aquatic toxicity testing of difficult substances and mixtures. OECD Series on Testing and Assessment. OECD, Paris. Available from: https://www.oecd.org/env/guidance-document-on-aquatic-toxicity-testing-of-difficult-substances-and-mixtures-0ed2f88e-en.htm
Parolini M, De Felice B, Ferrario C, Salgueiro-González N, Castiglioni S, Finizio A, Tremolada P, 2018. Benzoylecgonine exposure induced oxidative stress and altered swimming behavior and reproduction in Daphnia magna. Environ. Pollut. 232:236-244.
DOI: https://doi.org/10.1016/j.envpol.2017.09.038
Picado A, Chankova S, Fernandes A, Simões F, Leverett D, Johnson I, Hernan R, Pires AM, Matos J, 2007. Genetic variability in Daphnia magna and ecotoxicological evaluation. Ecotoxicol. Environ. Saf. 67:406-410.
DOI: https://doi.org/10.1016/j.ecoenv.2006.10.004
Pyle G, Ford AT, 2017. Behaviour revised: contaminant effects on aquatic animal behaviour. Aquat. Toxicol. 182:226–228.
DOI: https://doi.org/10.1016/j.aquatox.2016.11.008
R Development Core Team, 2020, R: A language and Environment for Statistical Computing. The R Foundation for Statistical Computing, Vienna.
Ren ZM, Li ZL, Zha, JM, Rao KF, Ma M, Wang Z, Fu RS, 2009. The avoidance responses of Daphnia magna to the exposure of organophosphorus pesticides in an on-line biomonitoring system. Environ. Model Assess. 14:405–410.
DOI: https://doi.org/10.1007/s10666-007-9136-0
Ren Z, Zha J, Ma M, Wang Z, Gerhardt A, 2007. The early warning of aquatic organophosphorus pesticide contamination by on-line monitoring behavioral changes of Daphnia magna. Environ. Monit. Assess. 134:373–383.
DOI: https://doi.org/10.1007/s10661-007-9629-y
Ritz C, Streibig JC, 2005. Bioassay analysis using R. J. Stat. Softw. 12:1-22.
DOI: https://doi.org/10.18637/jss.v012.i05
Rizzi C, Finizio A, Maggi V, Villa S, 2019. Spatial-temporal analysis and risk characterisation of pesticides in Alpine glacial streams. Envir. Poll. 248:659- 66.
DOI: https://doi.org/10.1016/j.envpol.2019.02.067
Saaristo B, Tomas Balshine S, Bertram MG, Brooks BW, Ehlman MS, McCallum ES, Sih A, Sundin J, Wong BMB Arnold KE, 2018. Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife. P. Roy. Soc. B-Biol. Sci. 285:20181297.
DOI: https://doi.org/10.1098/rspb.2018.1297
Scholze M, Boedeker W, Faust M, Backhaus T, Altenburger R, Grimme LH, 2001. A general best-fit method for concentration-response curves and the estimation of low-effect concentrations. Environ. Toxicol. Chem. 20: 448-457.
DOI: https://doi.org/10.1002/etc.5620200228
Sloman KA, McNeil PL, 2012. Using physiology and behaviour to understand the responses of fish early life stages to toxicants. J. Fish. Biol. 81:2175e2198.
DOI: https://doi.org/10.1111/j.1095-8649.2012.03435.x
Stamatis N, Hela D, Triantafyllidis V, Konstantinou I, 2013. Spatiotemporal variation and risk assessment of pesticides in water of the lower catchment basin of Acheloos River, western Greece. ScientificWorldJournal 2013:231610.
DOI: https://doi.org/10.1155/2013/231610
Tremolada P, Finizio A, Villa S, Gaggi C, Vighi M, 2004. Quantitative inter-specific chemical activity relationships of pesticides in the aquatic environment. Aquat. Toxicol. 67:87-103.
DOI: https://doi.org/10.1016/j.aquatox.2003.12.003
Verhaar HJM, van Leeuwen CJ, Hermens JLM, 1992. Classifying environmental pollutants. 1: Structure–activity relationships for prediction of aquatic toxicity. Chemosphere 25:471-491.
DOI: https://doi.org/10.1016/0045-6535(92)90280-5
Villa S, Negrelli C, Finizio A, Flora O, Vighi M, 2006. Organochlorine compounds in ice melt water from Italian Alpine rivers. Ecotox. Environ. Saf. 63:84-90.
DOI: https://doi.org/10.1016/j.ecoenv.2005.05.010
Villa S, Di Nica V, Pescatore T, Bellamoli F, Miari F, Finizio A, Lencioni V, 2018. Comparison of the behavioural effects of pharmaceuticals and pesticides on Diamesa zernyi larvae (Chironomidae). Environ. Pollut. 238:130–139.
DOI: https://doi.org/10.1016/j.envpol.2018.03.029
Villa S, Maggioni D, Hamza H, Di Nica V, Magni S, Morosetti B, Parenti CC, Finizio A, Binelli A, Della Torre C, 2020. Natural molecule coatings modify the fate of cerium dioxide nanoparticles in water and their ecotoxicity to Daphnia magna. Environ. Pollut. 257:113597.
DOI: https://doi.org/10.1016/j.envpol.2019.113597
Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Reidy Liermann C, Davies PM, 2010. Global threats to human water security and river biodiversity. Nature 467: 555-561.
DOI: https://doi.org/10.1038/nature09440
Wolf G, Scheunders P, Selens M, 1998. Evaluation of the swimming activity of D. magna by image analysis after administration of sublethal cadmium concentrations. Comp. Biochem. Phys. A 120:99-105.
DOI: https://doi.org/10.1016/S1095-6433(98)10016-8
Xuereb B, Lefèvre E, Garric J, Geffard O, 2009. Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): linking AChE inhibition and behavioural alteration. Aquat. Toxicol. 94:114-122.
DOI: https://doi.org/10.1016/j.aquatox.2009.06.010
Zein MA, McElmurry SP, Kashian DR, Savolainen PT, Pitts DK, 2014. Optical bioassay for measuring sublethal toxicity of insecticides in Daphnia pulex. Environ. Toxicol Chem. 33:144-151.
DOI: https://doi.org/10.1002/etc.2404
Zein MA, Mcelmurry SP, Kashian DR, Savolainen PT, Pitts DK, 2015. Toxic effects of combined stressors on Daphnia pulex: Interactions between diazinon, 4-nonylphenol, and wastewater effluent. Environ. Toxicol. Chem. 34:1145-1153.
DOI: https://doi.org/10.1002/etc.2908
Edited by
Ester Eckert, CNR-IRSA Verbania, ItalyHow to Cite
Di Nica, Valeria, Cristiana Rizzi, Antonio Finizio, Lorenzo Ferraro, and Sara Villa. 2021. “Behavioural Responses of Juvenile <i>Daphnia magna< i> To Two Organophosphorus Insecticides”. Journal of Limnology 81 (1). https://doi.org/10.4081/jlimnol.2021.2015.
Copyright (c) 2021 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Similar Articles
- Armine Hayrapetyan, Gor Gevorgyan , Martin Schultze, Muhammed Shikhani, Termine Khachikyan, Aleksandr Krylov, Karsten Rinke, Contemporary community composition, spatial distribution patterns, and biodiversity characteristics of zooplankton in large alpine Lake Sevan, Armenia , Journal of Limnology: Vol. 81 No. s1 (2022): Lake Sevan. Past, present, and future state of a unique alpine lake
- Andrea Gall, Martin J. Kainz, Serena Rasconi, Daphnia magna fitness during low food supply under different water temperature and brownification scenarios , Journal of Limnology: Vol. 76 No. 1 (2017)
- Sameer M. Padhye, Alexey A. Kotov, Neelesh Dahanukar, Henri Dumont, Biogeography of the ‘water flea’ Daphnia O. F. Müller (Crustacea: Branchiopoda: Anomopoda) on the Indian subcontinent , Journal of Limnology: Vol. 75 No. 3 (2016)
- Sara Villa, Valeria Di Nica, Francesco Bellamoli, Tanita Pescatore, Claudia Ferrario, Antonio Finizio, Valeria Lencioni, Effects of a treated sewage effluent on behavioural traits in Diamesa cinerella and Daphnia magna , Journal of Limnology: Vol. 77 No. s1 (2018): Recent advances in the study of Chironomidae: An overview
- Valeria Rossi, Catia Maurone, Giorgio Benassi, Silvia Marková, Petr Kotlík, Nicolò Bellin, Ireneo Ferrari, Phenology of Daphnia in a Northern Italy pond during the weather anomalous 2014 , Journal of Limnology: Vol. 74 No. 3 (2015)
- Johann P. Müller, David Laloi, Claude Yéprémian, Cécile Bernard, Florence D. Hulot, To flee or not to flee: detection, avoidance and attraction of profitable resources by Daphnia magna studied with olfactometer , Journal of Limnology: Vol. 72 No. 3 (2013)
- Silvia Marková, Catia Maurone, Erica Racchetti, Marco Bartoli, Valeria Rossi, Daphnia diversity in water bodies of the Po River Basin , Journal of Limnology: Vol. 76 No. 2 (2017)
- Marina Manca, Michela Rogora, Nico Salmaso, Inter-annual climate variability and zooplankton: applying teleconnection indices to two deep subalpine lakes in Italy , Journal of Limnology: Vol. 74 No. 1 (2015)
- Slawek Cerbin, Łukasz Wejnerowski, Marcin Dziuba, Aphanizomenon gracile increases in width in the presence of Daphnia. A defence mechanism against grazing? , Journal of Limnology: Vol. 72 No. 3 (2013)
- Pierluigi Colangeli, Adam Cieplinski, Ulrike Obertegger, Filming of zooplankton: a case study of rotifer males and Daphnia magna , Journal of Limnology: Vol. 75 No. 1 (2016)
You may also start an advanced similarity search for this article.
