Sulfate sensitivity of early life stages of freshwater mussels Unio crassus and Margaritifera margaritifera.

Bivalve Effective concentration Glochidia Osmotic stress Salinity Toxicity test

Journal

Ecotoxicology (London, England)
ISSN: 1573-3017
Titre abrégé: Ecotoxicology
Pays: United States
ID NLM: 9885956

Informations de publication

Date de publication:
08 Aug 2024
Historique:
accepted: 27 07 2024
medline: 8 8 2024
pubmed: 8 8 2024
entrez: 8 8 2024
Statut: aheadofprint

Résumé

Sulfate is increasingly found in elevated concentrations in freshwater ecosystems due to anthropogenic activities. Chronic exposure to sulfate has been reported to cause sublethal effects on freshwater invertebrates. Previous sulfate toxicity tests have mostly been conducted in hard or moderately hard waters, and research on species inhabiting soft water is needed, given that freshwater organisms face heightened sensitivity to toxicants in water of lower hardness. In the present study, we examined sulfate sensitivity of two endangered freshwater mussel species, Unio crassus, and Margaritifera margaritifera. Glochidia and juveniles of both species were subjected to acute and/or chronic sulfate exposures in soft water to compare sulfate sensitivity across age groups, and effective concentrations (EC)/lethal concentrations (LC) values were estimated. Mussels were individually exposed to allow relatively larger numbers of replicates per treatment. Chronic sulfate exposure significantly reduced growth, foot movement, and relative water content (RWC) in juvenile mussels of M. margaritifera. Mussels at younger stages were not necessarily more sensitive to sulfate. In the acute tests, LC50 of glochidia of M. margaritifera and U. crassus was 1301 and 857 mg/L, respectively. Chronic LC10 was 843 mg/L for 3-week-old U. crassus juveniles, 1051 mg/L for 7-week-old M. margaritifera juveniles, and 683 mg/L for 2-year-old M. margaritifera juveniles. True chronic Lowest Effective Concentration for 7-week-old M. margaritifera may be within the 95% interval of EC10 based on RWC (EC10 = 446 mg/L, 95%CI = 265-626 mg/L). Our study contributed to the understanding of sulfate toxicity to endangered freshwater mussel species in soft water.

Identifiants

pubmed: 39115797
doi: 10.1007/s10646-024-02794-4
pii: 10.1007/s10646-024-02794-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Arnér M, Koivisto S (1993) Effects of salinity on metabolism and life history characteristics of Daphnia magna. Hydrobiologia 259:69–77
doi: 10.1007/BF00008373
ASTM International (2022) Standard guide for conducting laboratory toxicity tests with freshwater mussels. ASTM 2022 E2455-22
Augspurger T, Keller AE, Black MC, Cope WG, Dwyer FJ (2003) Water quality guidance for protection of freshwater mussels (Unionidae) from ammonia exposure. Environ Toxicol Chem 22:2569–2575
doi: 10.1897/02-339
Barnhart M, Haag W, Roston W (2008) Adaptations to larval parasitism in the Unionoida. J-NABS 27:370–394. https://doi.org/10.1899/07-093.1
doi: 10.1899/07-093.1
Belamy T, Legeay A, Cachot J, Clérandeau C, Baudrimont M (2023) Locomotion behavior of juveniles of the freshwater pearl mussel Margaritifera margaritifera: a new non-invasive tool for the evaluation of stress effects. Chemosphere 327:138521. https://doi.org/10.1016/j.chemosphere.2023.138521
doi: 10.1016/j.chemosphere.2023.138521
Belamy T, Legeay A, Etcheverria B, Cordier MA, Gourves PY, Baudrimont M (2020) Acute toxicity of sodium chloride, nitrates, ortho-phosphates, cadmium, arsenic and aluminum for juveniles of the freshwater pearl mussel: Margaritifera margaritifera (L.1758). Environments 7:48
doi: 10.3390/environments7060048
Bernhardt ES, Palmer MA (2011) The environmental costs of mountaintop mining valley fill operations for aquatic ecosystems of the Central Appalachians. Ann N Y Acad Sci 1223:39–57
doi: 10.1111/j.1749-6632.2011.05986.x
Bringolf RB, Raines BK, Ratajczak RE, Haskins DL (2022) Major ion toxicity to glochidia of common and imperiled freshwater mussel species. Diversity 14(2):95. https://doi.org/10.3390/d14020095
doi: 10.3390/d14020095
Buchwalter D, Scheibener S, Chou H, Soucek D, Elphick J (2018) Are sulfate effects in the mayfly Neocloeon triangulifer driven by the cost of ion regulation? Philos Trans R Soc Lond B Biol Sci 374(1764):20180013. https://doi.org/10.1098/rstb.2018.0013
doi: 10.1098/rstb.2018.0013
Burton RF (1983) Ionic regulation and water balance. In: ASM Saleuddin and KM Wilbur (ed) The Mollusca. Academic Press, New York, pp 291–352
Bradley TJ (2009) Animal osmoregulation. Oxford University Press, Oxford
Cañedo-Argüelles M, Kefford B, Schäfer R (2019) Salt in freshwaters: causes, effects and prospects—introduction to the theme issue. Philos Trans R Soc Lond B Biol Sci 374(1764):20180002. https://doi.org/10.1098/rstb.2018.0002
doi: 10.1098/rstb.2018.0002
Cañedo-Argüelles M, Kefford B, Piscart C, Prat N, Schäfer R, Schulz C (2013) Salinisation of rivers: an urgent ecological issue. Environ Pollut 173:157–167
doi: 10.1016/j.envpol.2012.10.011
Crosa G, Froebrich J, Nikolayenko V, Stefani F, Galli P, Calamari D (2006) Spatial and seasonal variations in the water quality of the Amu Darya River (Central Asia). Water Res 40(11):2237–2245. https://doi.org/10.1016/j.watres.2006.04.004
doi: 10.1016/j.watres.2006.04.004
Davies T, Hall K (2007) Importance of calcium in modifying the acute toxicity of sodium sulphate to Hyalella azteca and Daphnia magna. Environ Toxicol Chem 26:1243–1247
doi: 10.1897/06-510R.1
de Renzis G, Maetz J (1973) Studies on the mechanism of chloride absorption by the goldfish gill: Relation with acid-base regulation. J Exp Biol 59:339–358
doi: 10.1242/jeb.59.2.339
Dietz TH, Udoetok AS, Cherry JS, Silverman H, Byrne RA (2000) Kidney function and sulfate uptake and loss in the freshwater bivalve Toxolasma texasensis. Biol Bull 199(1):14–20. https://doi.org/10.2307/1542702
doi: 10.2307/1542702
Dinno A (2017) conover.test: Conover-Iman Test of Multiple Comparisons Using Rank Sums. R package version 1.1.5, https://CRAN.R-project.org/package=conover.test .
EEA (2013a) Specie: Margaritifera margaritifera. Report under the Article 17 of the Habitats Directive Covering Period 2007–2012. European Topic Centre on Biological Diversity.
EEA (2013b) Specie: Unio crassus. Report under the Article 17 of the Habitats Directive Covering Period 2007–2012. European Topic Centre on Biological Diversity.
Ekholm P, Lehtoranta J, Taka M, Sallantaus T, Riihimäki J (2020) Diffuse sources dominate the sulfate load into Finnish surface waters. Sci Total Environ 748:141297. https://doi.org/10.1016/j.scitotenv.2020.141297
doi: 10.1016/j.scitotenv.2020.141297
Elphick J, Davies M, Gilron G, Canaria E, Lo B, Bailey H (2011) An aquatic toxicological evaluation of sulfate: The case for considering hardness as a modifying factor in setting water quality guidelines. Environ Toxicol Chem 30:247–253
doi: 10.1002/etc.363
Erickson RJ, Mount DR, Highland TL, Hockett JR, Hoff DJ, Jenson CT, Norberg-King TJ, Peterson KN (2017) The acute toxicity of major ion salts to Ceriodaphnia dubia. II. Empirical relationships in binary salt mixtures. Environ Toxicol Chem 36:1525–1537. https://doi.org/10.1002/etc.3669
doi: 10.1002/etc.3669
Ferreira-Rodríguez N, Akiyama YB, Aksenova OV et al. (2019) Research priorities for freshwater mussel conservation assessment. Biol Conserv 231:77–87
doi: 10.1016/j.biocon.2019.01.002
Gainey LF (1978) The response of the Corbiculidae (Mollusca: Bivalvia) to osmotic stress: the organismal response. Physiol Zool 51:68–78
doi: 10.1086/physzool.51.1.30158666
García-Romeu F, Maetz JG (1964) The mechanism of sodium and chloride uptake by the gills of a fresh-water fish, Carassius auratus: I. Evidence for an independent uptake of sodium and chloride ions. J Gen Physiol 47:1195–1207
doi: 10.1085/jgp.47.6.1195
Goodfellow W, Ausley L, Burton D, Denton D, Dorn P, Grothe D, Heber M, Norberg‐King T, Rodgers J (2000) Major ion toxicity in effluents: a review with permitting recommendations. Environ Toxicol Chem 19:175–182
doi: 10.1002/etc.5620190121
Griffith MB (2017) Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: teleost fish, crustacea, aquatic insects, and Mollusca. Environ Toxicol Chem 36(3):576–600. https://doi.org/10.1002/etc.3676
doi: 10.1002/etc.3676
Griffith MB, Lazorchak JM, Haring H (2020) Uptake of sulfate from ambient water by freshwater animals. Water 12(5):1–1496. https://doi.org/10.3390/w12051496
doi: 10.3390/w12051496
Hartmann J, Beggel S, Auerswald K, Stoeckle B, Geist J (2015) Establishing mussel behavior as a biomarker in ecotoxicology. Aquat Toxicol 170:279–288
doi: 10.1016/j.aquatox.2015.06.014
Hayward EE, Gillis PL, Bennett CJ, Prosser RS, Salerno J, Liang T, Robertson S, Metcalfe CD (2022) Freshwater mussels in an impacted watershed: Influences of pollution from point and non-point sources. Chemosphere 307:135966
doi: 10.1016/j.chemosphere.2022.135966
Helama S, Valovirta I (2008) The oldest recorded animal in Finland: ontogenetic age and growth in Margaritifera margaritifera (L. 1758) based on internal shell increments. Memoranda Soc Fauna Fl 84:20–30
Hyvärinen H, Sjönberg T, Marjomäki TJ, Taskinen J (2022) Effect of low dissolved oxygen on the survival of juvenile Margaritifera margaritifera: hypoxia tolerance ex situ. Aquat Conserv 32:1393–1400. https://doi.org/10.1002/aqc.3859
doi: 10.1002/aqc.3859
Johnson BR, Weaver PC, Nietch CT, Lazorchak JM, Struewing KA, Funk DH (2015) Elevated major ion concentrations inhibit larval mayfly growth and development. Environ Toxicol Chem 34(1):167–172. https://doi.org/10.1002/etc.277
doi: 10.1002/etc.277
Karjalainen J, Mäkinen M, Karjalainen AK (2021) Sulfate toxicity to early life stages of European whitefish (Coregonus lavaretus) in soft freshwater. Ecotoxicol Environ Saf 208:111–763. https://doi.org/10.1016/j.ecoenv.2020.111763
doi: 10.1016/j.ecoenv.2020.111763
Karjalainen J, Hu X, Mäkinen M, Karjalainen A, Järvistö J, Järvenpää K, Sepponen M, Leppänen MT (2023) Sulfate sensitivity of aquatic organism in soft freshwaters explored by toxicity tests and species sensitivity distribution. Ecotoxicol Environ Saf 258:114984. https://doi.org/10.1016/j.ecoenv.2023.114984
doi: 10.1016/j.ecoenv.2023.114984
Kefford BJ (2018) Why are mayflies (Ephemeroptera) lost following small increases in salinity? Three conceptual osmophysiological hypotheses. Philos Trans R Soc Lond B Biol Sci 374(1764):20180021. https://doi.org/10.1098/rstb.2018.0021
doi: 10.1098/rstb.2018.0021
Kennedy A, Cherry D, Currie R (2003) Field and laboratory assessment of a coal processing effluent in the leading creek watershed, Meigs county, Ohio. Arch Environ Contam Toxicol 44:0324–0331
doi: 10.1007/s00244-002-2062-x
Kennedy AJ, Cherry DS, Zipper CE (2005) Evaluation of Ionic Contribution to the Toxicity of a Coal-Mine Effluent Using Ceriodaphnia dubia. Arch Environ Contam Toxicol 49:155–162
doi: 10.1007/s00244-004-0034-z
Kunz J, Conley J, Buchwalter D, Norberg-King T, Kemble N, Wang N, Ingersoll C (2013) Use of reconstituted waters to evaluate effects of elevated major ions associated with mountaintop coal mining on freshwater invertebrates. Environ Toxicol Chem 32:2826–2835
doi: 10.1002/etc.2391
Lens P, Visser A, Janssen A, Hulshoff L, Lettinga G (1998) Biotechnological treatment of sulfate-rich wastewaters. Crit Rev Env Sci Tec 28:41–88
doi: 10.1080/10643389891254160
Lopes-Lima M, Sousa R, Geist J et al. (2017) Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92:572–607. https://doi.org/10.1111/brv.12244
doi: 10.1111/brv.12244
Lopes-Lima M, Kebapçı U, Van Damme D (2014) Unio crassus. The IUCN Red List of Threatened Species 2014: e.T22736A42465628. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T22736A42465628.en .
March FA, Dwyer FJ, Augspurger T, Ingersoll CG, Wang N, Mebane CA (2007) An evaluation of freshwater mussel toxicity data in the derivation of water quality guidance and standards for copper. Environ Toxicol Chem 26:2066–2074. https://doi.org/10.1897/06-560R.1
doi: 10.1897/06-560R.1
McMahon BR, Stuart SA (1989) The physiological problems of crayfish in acid waters. In: R Morris, EW Taylor, DJA Brown, JA Brown (ed) Acid Toxicity and Aquatic Animals, Vol 34—Society for Experimental Biology Seminar Series. Cambridge University, Cambridge, UK, p 171–199
McMahon RF, Bogan AE (2001) Chapter 11: Mollusca: Bivalvia. In: Thorp J and Covich A(ed) Ecology and classification of North American freshwater invertebrates, 2nd edn. Academic Press, p 297–329.
Mount DR, Gulley DD, Hockett JR, Garrison TD, Evans JM (1997) Statistical models to predict the toxicity of major ions to Ceriodaphnia dubia, Daphnia magna and Pimephales promelas (fathead minnows). Environ Toxicol Chem 16:2009–2019. https://doi.org/10.1002/etc.5620161005
doi: 10.1002/etc.5620161005
Mount DR, Erickson RJ, Highland TL, Hockett JR, Hoff DJ, Jenson CT, Norberg-King TJ, Peterson KN, Polaske ZM, Wisniewski S (2016) The acute toxicity of major ion salts to Ceriodaphnia dubia: I. Īnfluence of background water chemistry. Environ Toxicol Chem 35:3039–3057. https://doi.org/10.1002/etc.3487
doi: 10.1002/etc.3487
Muschal M (2006) Assessment of risk to aquatic biota from elevated salinity—a case study from the Hunter River, Australia. J Environ Manage 79:266–278. https://doi.org/10.1016/j.jenvman.2005.08.002
doi: 10.1016/j.jenvman.2005.08.002
Nyberg M, Österholm P, Nystrand M (2012) Impact of acid sulfate soils on the geochemistry of rivers in south-western Finland. Environ Earth Sci 66:157–168
doi: 10.1007/s12665-011-1216-4
OECD (2006) Current Approaches in the Statistical Analysis of Ecotoxicity Data: A guidance to application (annexes to this publication exist as a separate document), OECD Series on Testing and Assessment, No. 54, OECD Publishing, Paris, https://doi.org/10.1787/9789264085275-en
Ortmann C, Grieshaber M (2003) Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea. J Exp Biol 206:4167–4178
doi: 10.1242/jeb.00656
Oulasvirta P, Leinikki J, Syväranta J (2017) Freshwater pearl mussel in Finland—current status and future prospects. Biol Bull Russ Acad Sci 44(1):81–91. https://doi.org/10.1134/S1062359017010101
doi: 10.1134/S1062359017010101
Pond GJ, Passmore ME, Borsuk FA, Reynolds L, Rose CJ (2008) Downstream effects of mountaintop coal mining: Comparing biological conditions using family- and genus-level macroinvertebrate bioassessment tools. J-NABS 27:717–737. https://doi.org/10.1899/08-015.1
doi: 10.1899/08-015.1
Riisgård HU, Larsen PS (2015) Physiologically regulated valve-closure makes mussels long-term starvation survivors: test of hypothesis. J Molluscan Stud 81:303–307
doi: 10.1093/mollus/eyu087
Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PloS one 10(12):e0146021
doi: 10.1371/journal.pone.0146021
Rivera-Ingraham GA, Lignot J (2017) Osmoregulation, bioenergetics and oxidative stress in coastal marine invertebrates: Raising the questions for future research. J Exp Biol 220(10):1749–1760. https://doi.org/10.1242/jeb.135624
doi: 10.1242/jeb.135624
Ruiz JL, Souza M (2008) Osmotic stress and muscle tissue volume response of a freshwater bivalve. Comp Biochem Physiol A Mol Integr Physiol 151:399–406
doi: 10.1016/j.cbpa.2007.03.028
Runtti H, Tolonen E, Tuomikoski S, Luukkonen T, Lassi U (2018) How to tackle the stringent sulfate removal requirements in mine water treatment—a review of potential methods. Environ Res 167:207–222. https://doi.org/10.1016/j.envres.2018.07.018
doi: 10.1016/j.envres.2018.07.018
Schartum E, Mortensen S, Pittman K, Jakobsen PJ (2017) From pedal to filter feeding: ctenidial organogenesis and implications for feeding in the postlarval freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758). J Molluscan Stud 83:36–42
doi: 10.1093/mollus/eyw037
Scheibener S, Conley JM, Buchwalter D (2017) Sulfate transport kinetics and toxicity are modulated by sodium in aquatic insects. Aquat Toxicol 190:62–69. https://doi.org/10.1016/j.aquatox.2017.06.027
doi: 10.1016/j.aquatox.2017.06.027
Shaw J (1960) The absorption of sodium ions by the crayfish, Astacus pallipes Lereboullet: II. The effect of the external anion. J Exp Biol 37:534–547
doi: 10.1242/jeb.37.3.534
Skinner A, Young M, Hastie L (2003) Ecology of the freshwater pearl mussel. Conserving Natura 2000 Rivers Ecology Series No. 2 English Nature, Peterborough
Soucek D (2007b) Bioenergetic effects of sodium sulfate on the freshwater crustacean, Ceriodaphnia dubia. Ecotixocol 16:317–325
Soucek D (2007a) Sodium sulfate impacts feeding, specific dynamic action, and growth rate in the freshwater bivalve Corbicula fluminea. Aquat Toxicol 83:315–322
doi: 10.1016/j.aquatox.2007.05.006
Soucek D, Kennedy A (2005) Effects of hardness, chloride, and acclimation on the acute toxicity of sulfate to freshwater invertebrates. Environ Toxicol Chem 24:1204–1210
doi: 10.1897/04-142.1
van Dam R, Harford A, Lunn S, Gagnon M (2014) Identifying the cause of toxicity of a saline mine water. PLoS One 9:e106857
doi: 10.1371/journal.pone.0106857
Vaughn C, Nichols S, Spooner D (2008) Community and foodweb ecology of freshwater mussels. J-NABS 27:409–423
Velasco J, Gutiérrez-Cánovas C, Botella-Cruz M et al. (2019) Effects of salinity changes on aquatic organisms in a multiple stressor context. Philos Trans R Soc Lond B Biol Sci 374(1764):20180011. https://doi.org/10.1098/rstb.2018.0011
doi: 10.1098/rstb.2018.0011
Wächtler K, Dreher-Mansur MC, Richter T (2001) Larval types and early postlarval biology in naiads (Unionoida). In: G Bauer and K Wächtler (ed) Ecology and Evolution of the Freshwater Mussels Unionoida. Ecological Studies, Vol. 145, Springer-Verlag Berlin Heidelberg
Wang N, Kunz JL, Hardesty DK et al. (2021) Method development for a short-term 7-day toxicity test with Unionid mussels. Environ Toxicol Chem 40:3392–3409. https://doi.org/10.1002/etc.5225
doi: 10.1002/etc.5225
Wang N, Dorman RA, Ivey CD, Soucek DJ, Dickinson A, Kunz BK, Bauer CR (2020) Acute and chronic toxicity of sodium nitrate and sodium sulfate to several freshwater organisms in water‐only exposures. Environ Toxicol Chem 39:1071–1085
doi: 10.1002/etc.4701
Wang N, Dorman R, Ingersoll C, Hardesty D, Brumbaugh W, Hammer E, Bauer C, Mount D (2016) Acute and chronic toxicity of sodium sulfate to four freshwater organisms in water-only exposures. Environ Toxicol Chem 35:115–127
doi: 10.1002/etc.3148
Wang N, Ingersoll CG, Ivey CD, Hardesty DK, May TW, Augspurger T, Roberts AD, van Genderen E, Barnhart MC (2010) Sensitivity of early life stages of freshwater mussels (Unionidae) to acute and chronic toxicity of lead, cadmium, and zinc in water. Environ Toxicol Chem 29:2053–2063
doi: 10.1002/etc.250
Wang N, Ivey CD, Ingersoll CG, Brumbaugh WG, Alvarez D, Hammer EJ, Bauer CR, Augspurger T, Raimondo S, Barnhart (2017) Acute sensitivity of a broad range of freshwater mussels to chemicals with different modes of toxic action. Environ Toxicol Chem 36:786–796
doi: 10.1002/etc.3642
Wang N, Ingersoll CG, Hardesty DK, Ivey CD, Kunz JL, May TW, Dwyer FJ, Roberts AD, Augspurger T, Kane CM, Neves RJ, Barnhart MC (2007) Acute toxicity of copper, ammonia, and chlorine to glochidia and juveniles of freshwater mussels (Unionidae). Environ Toxicol Chem 26:2036–2047
doi: 10.1897/06-523R.1
Williams D, Williams NE, Cao Y (2000) Road salt contamination of groundwater in a major metropolitan area and development of a biological index to monitor its impact. Water Res 34:127–138. https://doi.org/10.1016/S0043-1354(99)00129-3
doi: 10.1016/S0043-1354(99)00129-3

Auteurs

Xiaoxuan Hu (X)

University of Jyväskylä, Department of Biological and Environmental Science, Jyväskylä, Finland. xhux@jyu.fi.

Mikko Mäkinen (M)

University of Jyväskylä, Department of Biological and Environmental Science, Jyväskylä, Finland.

Jouni Taskinen (J)

University of Jyväskylä, Department of Biological and Environmental Science, Jyväskylä, Finland.

Juha Karjalainen (J)

University of Jyväskylä, Department of Biological and Environmental Science, Jyväskylä, Finland.

Classifications MeSH