Abstract
We identified publication trends and methodological changes in polychaete ecotoxicological studies since the review carried out by Reish and Gerlinger (Bull Mar Sci 60:584–607, 1997) using a classic review approach. We also carried out a meta-analysis to identify the overall effect of the type of pollutants (e.g., hydrocarbons, metals, pesticides) and to test the consistency of their effect at different levels of analysis (e.g., biochemical, physiological, behavioral) using 14 different biological responses (e.g., bioaccumulation, tolerance, enzymatic activity). A total of 136 articles met the selection criteria and were analyzed for the classic review. Main findings include: (1) studies focused on the effects of metals (48%), hydrocarbons (32%), and pesticides (20%); (2) sublethal effects were more frequent; and (3) the nereidid species Hediste diversicolor was the most studied species. For the meta-analysis, 27 articles met the selection criteria and a total of 168 effect sizes were calculated. The results from the generalized linear mixed models (GLMMs) indicated that the hydrocarbons have the strongest effect in polychaetes, while the most sensitive metric is behavior. Enzymatic activity and mortality represented the most sensitive biological responses to estimating the magnitude and direction of the effect. Finally, the tendencies observed in the classic review did not represent the strongest effects in the GLMMs.
Similar content being viewed by others
References
Bridges TS, Levin LA, Cabrera D, Plaia G (1994) Effects of sediment amended with sewage, algae, or hydrocarbons on growth and reproduction in two opportunistic polychaetes. J Exp Mar Bio Ecol 177:99–119. https://doi.org/10.1016/0022-0981(94)90146-5
Colvin MA, Hentschel BT, Deheyn DD (2016) Combined effects of water flow and copper concentration on the feeding behavior, growth rate, and accumulation of copper in tissue of the infaunal polychaete Polydora cornuta. Ecotoxicology 25:1720–1729. https://doi.org/10.1007/s10646-016-1705-z
Conover WJ (1999) Practical Nonparametric Statistics, 3rd Edition. ISBN: 978-0-471-16068-7. pp. 608.
Dean HK (2008) The use of polychaetes (Annelida) as indicator species of marine pollution: a review. Rev Biol Trop 56(4):11–38.
Fernández-Rodríguez V, Santos CS, Pires APF (2019) Meta-analysis of the effects of organic matter on polychaetes of the east coast of South America. Mar Environ Res 149:148–156. https://doi.org/10.1016/j.marenvres.2019.06.001
Foss H, Forbes V (1997) Effects of the polycyclic aromatic hydrocarbon fluoranthene on growth rate and nucleic acid composition of Capitella sp. I Mar Biol 129:489–497. https://doi.org/10.1007/s002270050189
Freire MM, Santos VG, Ginuino ISF, Arias ARL (2008) Biomarcadores na avaliação da saúde ambiental dos ecossistemas aquáticos. Oecologia Brasiliensis 12(3):347–354.
Giger W (2009) Hydrophilic and amphiphilic water pollutants using advanced analytical methods for classic and emerging contaminants. Anal Bioanal Chem 393(1):37–44.
Hampel M, Blasco J, Segner H (2015) Molecular and cellular effects of contamination in aquatic ecosystems. Environ Sci Pollut Res 22(22):17261–17266. https://doi.org/10.1007/s11356-015-5565-5
Holmer M, Forbes VE, Forbes TL (1997) Impact of the polychaete Capitella sp. I on microbial activity in an organic-rich marine sediment contaminated with the polycyclic aromatic hydrocarbon fluoranthene. Mar Biol 128:679–688. https://doi.org/10.1007/s002270050135
Hutchings P (1998) Biodiversity and functioning of polychaetes in benthic sediments. Biodivers Conserv 7:1133–1145. https://doi.org/10.1023/A:1008871430178
Jennions M, Lortie C, Rosenberg M, Rothstein H (2013) Publication and related biases. In: Koricheva J, Gurevitch J, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton, pp 206–236.
Lajeunesse MJ (2013) Recovering missing or partial data from studies: a survey of conversions and imputations for meta-analysis. In: Koricheva J, Gurevitch J, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton, pp 195–206.
Langston WJ, Bebianno MJ, Burt GR (1998) Metal handling strategies in molluscs. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments. Chapman and Hall, London, pp 219–283.
Martínez-Jerónimo M, Cruz-Cisneros JL, García-Hernández L (2008) A comparison of the response of Simocephalus mixtus (Cladocera) and Daphnia magna to contaminated freshwater sediments. Ecotoxicol Environ Saf 71:26–31. https://doi.org/10.1016/j.ecoenv.2008.05.005
Mengersen K, Schmid C (2013) Maximum likelihood approaches. In: Koricheva Julia et al (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton, pp 125–144.
Metian M, Hédouin L, Oberhänsli F, Warnau M (2009) Delineation of heavy metal uptake pathways (seawater and food) in the variegated scallop Chlamys varia using radiotracer techniques. Mar Ecol Prog Ser. https://doi.org/10.3354/meps07766
O’Callaghan I, Fitzpatrick D, Sullivan T (2022) Thiophilicity is a determinant of bioaccumulation in benthic fauna. Environ Pollut. 294:118641. https://doi.org/10.1016/j.envpol.2021.118641
Oliva M, Vicente JJ, Gravato C, Guilhermino L, Galindo-Riaño MD (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotoxicol Environ Saf 75(1):151–162. https://doi.org/10.1016/j.ecoenv.2011.08.017
Palmqvist A, Selck H, Rasmussen LJ, Forbes VE (2003) Biotransformation and genotoxicity of fluoranthene in the deposit-feeding polychaete Capitella sp. I Environ Toxicol Chem 22(12):2977–2985. https://doi.org/10.1897/02-474
Perelo LW (2010) Review: In situ and bioremediation of organic pollutants in aquatic sediments. J Hazard Mater 177:81–89. https://doi.org/10.1016/j.jhazmat.2009.12.090
Pocklington P, Wells PG (1992) Polychaetes e Key taxa for marine environmental quality monitoring. Mar Poll Bull 24:593–598. https://doi.org/10.1016/0025-326X(92)90278-E
Reish DJ, Gerlinger TV (1997) A review of the toxicological studies with polychaetous annelids. Bull Mar Sci 60(2):584–607.
Riba I, Casado-Martínez C, Forja JM, DelValls A (2004) Sediment quality in the Atlantic coast of Spain. Environ Toxicol Chem 23(2):271–282. https://doi.org/10.1897/03-146
Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59(2):464–468.
Rosenberg M (2013) Effect sizes: conventional choices and calculations. In: Rosenberg M, Rothstein H, Stewart GB, Koricheva J, Gurevitch J, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton.
Rosenberg MS (2022) MetaWin 3. https://metawindoft.com
Sun F, Zhou Q (2008) Oxidative stress biomarkers of the polychaete Nereis diversicolor exposed to cadmium and petroleum hydrocarbons. Ecotoxicol Environ Saf 70:106–114. https://doi.org/10.1016/j.ecoenv.2007.04.014
Surugiu V (2005) The use of polychaetes as indicators of eutrophication and organic enrichment of coastal waters: a study case–romanian black sea coast. Analele Ştiinţifice ale Universităţii “Al.I. Cuza” Iaşi, s. Biologie Animală 51:55–62.
Won EJ, Kim RO, Rhee JS, Park GS, Lee J, Shin KH, Lee YM, Lee JS (2011) Response of glutathione S-transferase (GST) genes to cadmium exposure in the marine pollution indicator worm. Perinereis Nuntia Comp Biochem Physiol Part C 154:82–92. https://doi.org/10.1016/j.cbpc.2011.03.008
Won EJ, Rhee JS, Ra K, Kim KT, Au DWT, Shin KH, Lee LS (2012) Molecular cloning and expression of novel metallothionein (mt) gene in the polychaete Perinereis nuntia exposed to metals. Environ Sci Pollut Res 19(7):2606–2618. https://doi.org/10.1007/s11356-012-0905-1
Yuan X, Chen A, Zhou Y, Liu H, Yang D (2010) The influence of cadmium on the antioxidant enzyme activities in polychaete Perinereis aibuhitensis Grube (Annelida: Polychaeta). Chin. J. Oceanol. Limnol. 28:849–855. https://doi.org/10.1007/s00343-010-9127-x
Zheng S, Chen B, Wanga Z, Qiu X, Yu X, Freestone D, Liu Z, Huang H, Yu W, Xu X (2010) Reproductive toxic effects of sublethal cadmium on the marine polychaete Perinereis nuntia. Ecotoxicol Environ Saf 73:1196–1201. https://doi.org/10.1016/j.ecoenv.2010.05.022
Acknowledgements
This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)-Finance Code 001. We thank Dr. Michael S. Rosenberg, from Virginia Commonwealth University, for sharing the beta version of MetaWin 3.0.6., and Dr. Mary Colleen Hannon, Smithsonian National Museum of Natural History, for proofreading the manuscript. The authors are grateful to the anonymous reviewers whose comments greatly improved this work.
Author information
Authors and Affiliations
Contributions
TMA conceived the original idea, designed and conducted the data search, organized data, proposed categories in the meta-analysis, conducted the classic review, and interpreted the results. VFR designed and conducted the meta-analysis and interpreted and discussed results. CSGS structured the idea, interpreted results, and contributed with advice in Annelida knowledge. TMA, VFR, and CSGS wrote the manuscript and contributed to the discussion. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of Interests
The authors declare that there is no conflict of interest in this publication.
Additional information
Communicated by Vinicius Farjalla.
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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Medeiros Aguiar, T., Fernández-Rodríguez, V. & Gomes Santos, C.S. Dirty workers: What do we know about the ecotoxicological studies in polychaetes?. Aquat Ecol 57, 783–796 (2023). https://doi.org/10.1007/s10452-023-10049-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-023-10049-3