Abstract
Salinization in freshwaters is gradually increasing as a result of human activities and climatic changes. Higher salt content causes stress for freshwater organisms. Sodium chloride (NaCl) is among the most frequently occurring salts in freshwater ecosystems. The objective of the present study was to investigate the lethal and sublethal effects of NaCl on freshwater ecosystems, using as test organism the dipteran Chironomus xanthus and the planarian Girardia tigrina. Acute tests showed that C. xanthus was more sensitive (48-h LC50 (median lethal concentration) of 2.97 g NaCl L−1) than G. tigrina (48-h LC50 of 7.77 g NaCl L−1). C. xanthus larvae growth rate (larvae length and head capsule width) was significantly reduced under exposure to concentrations as low as 0.19 g L−1 NaCl and higher. A delay in the emergence time (EmT50) was also demonstrated for the same concentration. Sublethal NaCl effects in G. tigrina included feeding inhibition (LOEC (lowest observed effect concentration) of 0.4 g L−1), reduced locomotion (LOEC = 0.2 g L−1), and 24–48-h blastema regeneration (LOEC = 0.2 g L−1 and 0.1 g L−1, respectively). The results demonstrated the toxicity of NaCl to C. xanthus and G. tigrina including sublethal effects that can result in negative consequences for populations in natural freshwaters under salinization.
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References
ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E −729–80. American Standards for Testing and Materials, Philadelphia, P.A
Balushkina EV, Golubkov SM, Golubkov MS, Litvinchuk LF, Shadrin NV (2009) Effect of abiotic and biotic factors on the structural and functional organization of the saline lake ecosystems. Zh Obshch Biol 70:504–514
Benbow ME, Merritt RW (2004) Road-salt toxicity of select michigan wetland macroinvertebrates under different testing conditions. Wetlands 24:68–76. https://doi.org/10.1672/0277-5212(2004)024[0068:RTOSMW]2.0.CO;2
Berezina NA (2003) Tolerance of freshwater invertebrates to changes in water salinity. Russ J Ecol 34:261–266. https://doi.org/10.1023/A:1024597832095
Bonada N, Prat N, Resh VH, Statzner B (2006) Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annu Rev Entomol 51:495–523. https://doi.org/10.1146/annurev.ento.51.110104.151124
Cañedo-Argüelles M, Kefford BJ, Piscart C, Prat N, Schafer RB, Schulz CJ (2013) Salinisation of rivers: an urgent ecological issue. Environ Pollut 173:157–167. https://doi.org/10.1016/j.envpol.2012.10.011
Cañedo-Argüelles M, Sala M, Peixoto G, Prat N, Faria M, Soares AMVM, Barata C, Kefford B (2015) Can salinity trigger cascade effects on streams? A mesocosm approach. Sci Total Environ 540:3–10. https://doi.org/10.1016/j.scitotenv.2015.03.039
Cartier V, Claret C, Garnier R, Franquet E (2011) How salinity affects life cycle of a brackish water species, Chironomus salinarius Kieffer (Diptera:Chironomidae). J Exp Mar Biol Ecol 405:93–98. https://doi.org/10.1016/j.jembe.2011.05.019
Dornelas ASP, Sarmento RA, Silva LCR, Saraiva AS, Souza DJ, Bordalo MD, Soares AMVM, Pestana JLT (2020) Toxicity of microbial insecticides towards the non-target freshwater insect Chironomus xanthus. Pest Manag Sci 75:1–27. https://doi.org/10.1002/ps.5629
Drake P, Arias AM (1995) Distribution and production of Chironomus salinarius (Diptera, Chironomidae) in a shallow coastal lagoon in the Bay of Cadiz. Hydrobiologia 299:195–206. https://doi.org/10.1007/BF00767326
El-Shabrawy GM, El Sayed TR (2005) Long-term changes and community structure of macrobenthic Arthropoda and Mollusca in Bardawill lagoon. Thalassia Salent 28:17–30. https://doi.org/10.1285/i15910725v28p17
Ferreira-Junior DF, Sarmento RA, Saraiva AS, Pereira RR, Picanço MC, Pestana JLT, Soares AMVM (2017) Low Concentrations of glyphosate-based herbicide affects the development of Chironomus xanthus. Water Air Soil Pollut 228:1–8. https://doi.org/10.1007/s11270-017-3536-9
Ferreira-Junior DF, Sarmento RA, Saraiva AS, Dornelas ASP, Pestana JLT, Soares AMVM (2018) Effects of a thiamethoxam-based insecticide on the life history of Chironomus xanthus. Water Air Soil Pollut 229:1–8. https://doi.org/10.1007/s11270-018-3994-8
Ferrington LC (2008) Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiologia 595:447–455. https://doi.org/10.1007/s10750-007-9130-1
Ghazy MMED, Habashy MM, Kossa FI, Mohammady EY (2009) Effects of salinity on survival, growth and reproduction of the water flea, Daphnia magna. Nat Sci 7:28–42
Gillis PL (2011) Assessing the toxicity of sodium chloride to the glochidia of freshwater mussels: Implications for salinization of surface waters. Environ Pollut 159:1702–1708. https://doi.org/10.1016/j.envpol.2011.02.032
Grzesiuk M, Mikulski A (2006) The effects of salinity on freshwater crustaceans. Pol J Ecol 54:669–674
Hasan MM, Defaveri J, Kuure S, Dash SN, Lehtonen S, Merilä J, Mccairns RJS (2017) Sticklebacks adapted to divergent osmotic environments show differences in plasticity for kidney morphology and candidate gene expression. J Exp Biol 220:2175–2186. https://doi.org/10.1242/jeb.146027
Hassell KL, Kefford BJ, Nugegoda D (2006) Sub-lethal and chronic salinity tolerances of three freshwater insects: Cloeon sp. and Centroptilum sp. (Ephemeroptera: Baetidae) and Chironomus sp. (Diptera: Chironomidae). J Exp Biol 209:4024–4032. https://doi.org/10.1242/jeb.02457
Hunt M, Herron E, Green L (2012) Chlorides in fresh water. URI watershed Watch: URIWW 4:3
Inoue T, Kumamoto H, Okamoto K, Umesono Y, Sakai M, Alvarado AS, Agata K (2004) Morphological and functional recovery of the planarian photosensing system during head regeneration. Zool Sci 21:275–283. https://doi.org/10.2108/zsj.21.275
Inoue T, Hoshino H, Yamashita T, Shimoyama S, Agata K (2015) Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function. Zool Lett 1:1–15. https://doi.org/10.1186/s40851-014-0010-z
Kaushal SS, Likens GE, Pace ML, Utz RM, Haq S, Gorman J, Grese M (2018) Freshwater salinization syndrome on a continental scale. Proc Natl Acad Sci 115:574–583. https://doi.org/10.1073/pnas.1711234115
Kefford BJ, Buchwalter D, Cañedo-Argüelles M, Davis J, Duncan RP, Hoffmann A, Thompson R (2016) Salinized rivers: degraded systems or new habitats for salttolerant faunas? Biol Lett 12:1–7. https://doi.org/10.1098/rsbl.2015.1072
Knakievicz T (2014) Planarians as invertebrate bioindicators in freshwater environmental quality: the biomarkers approach. Ecotoxicol Environ Contam 9:1–12. https://doi.org/. https://doi.org/10.5132/eec.2014.01.001
Knakievicz T, Ferreira H (2008) Evaluation of copper effects upon Girardia tigrina freshwater planarians based on a set of biomarkers. Chemosphere 71:419–428. https://doi.org/10.1016/j.chemosphere.2007.11.004
Knakievicz T, Ertdmann B, Vieira SM, Ferreira HB (2006) Reproduction modes and life cycle of freshwater planarians (Plathyhelminthes, Tricladida, Paludicula) from Southern Brazil. Invertebr Biol 125:212–221. https://doi.org/10.1111/j.1744-7410.2006.00054.x
Kokkinn MJ, Williams WD (1988) Adaptations to life in a hypersaline water-body: adaptations at the egg and early embryonic stage of Tanytarsus barbitarsis Freeman (Diptera, Chironomidae). Aquat Insects 10:205–214. https://doi.org/10.1080/01650428809361331
Legner EF, Tsai TC, Medved RA (1976) Environmental stimulants to asexual reproduction in the planarian, Dugesia dorotocephala. Entomophaga 21:415–423. https://doi.org/10.1007/BF02371640
Lopes I, Moreira SM, Da Silva E, Sousa J, Guilhermino L, Soares A, Ribeiro R (2007) In situ assays with tropical cladocerans to evaluate edge-of-field pesticide runoff toxicity. Chemosphere 67:2250–2256. https://doi.org/10.1016/j.chemosphere.2006.12.009
López AMC, Sarmento RA, Saraiva ASS, Pereira RR, Soares AMVM, Pestana JLT (2019) Exposure to Roundup® affects behaviour, head regeneration and reproduction of the freshwater planarian Girardia tigrina. Sci Total Environ 675:453–461. https://doi.org/10.1016/j.scitotenv.2019.04.234
Macêdo LPR, Dornelas ASP, Vieira MM, Ferreira JSJ, Sarmento RA, Cavallini GS (2019) Comparative ecotoxicological evaluation of peracetic acid and the active chlorine of calcium hypochlorite: Use of Dugesia tigrina as a bioindicator of environmental pollution. Chemosphere 233:273–281. https://doi.org/10.1016/j.chemosphere.2019.05.286
Moreira SS, Zuanon J (2002) Dieta de Retroculus lapidifer (Perciformes: Cichlidae), um peixe reofílico do rio Araguaia, estado do Tocantins, Brasil. Acta Amaz 32:691–705
Nano GM, Binelloa A, Biancob AM, Ugazioc G, Burdino S (2002) In vitro tests to evaluate potential biological activity in natural substances. Fitoterapia 73:140–146. https://doi.org/10.1016/S0367-326X(02)00014-X
Neumann B, Vafeidis AT, Zimmermann J, Nicholls RJ (2015) Future coastal population growth and exposure to sea-level rise and coastal flooding - a global assessment. PLoS One 10:e0118571. https://doi.org/10.1371/journal.pone.0118571
Nogueira G, Stigter TY, Zhou Y, Mussa F, Juizo D (2019) Understanding groundwater salinization mechanisms to secure freshwater resources in the water-scarce city of Maputo, Mozambique. Sci Total Environ 661:723–736. https://doi.org/10.1016/j.scitotenv.2018.12.343
Novelli A, Vieira BH, Cordeiro D, Cappelini LTD, Vieira EM, Espíndola ELG (2012) Lethal effects of abamectin on the aquatic organisms Daphnia similis, Chironomus xanthus and Danio rerio. Chemosphere 86:36–40. https://doi.org/10.1016/j.chemosphere.2011.08.047
NRCC - National Research Council of Canada (1977) The effects of alkali halides in the Canadian environment. Associate Committee on Scientific Criteria for Environmental Quality, National Research Council of Canada, Ottawa (Publication NRCC No. 15019)
Nutile SA, Solan ME (2019) Toxicity testing of “eco-friendly” de-icing formulations using Chironomus dilutus. Environ Pollut 246:408–413. https://doi.org/10.1016/j.envpol.2018.12.033
OECD - Organization for Economic Cooperation and Development (2004) Guidelines for the Testing of Chemicals. In: Section 2. Effects on Biotic Systems Test n°. 219: Sediment-water chironomid toxicity using spiked water. Paris, France
OECD - Organization for Economic Cooperation and Development (2011) Guidelines for the Testing of Chemicals. In: Section 2. Effects on Biotic Systems. Test n°. 234: Fish sexual development test. Paris, France
Ofoegbu PU, Simão FCP, Cruz A, Mendo S, Soares AMVM, Pestana JLT (2016) Toxicity of tributyltin (TBT) to the freshwater planarian Schmidtea mediterranea. Chemosphere 148:61–67. https://doi.org/10.1016/j.chemosphere.2015.12.131
Ofoegbu PU, Campos D, Soares AMVM, Pestana JLT (2019) Combined effects of NaCl and fluoxetine on the freshwater planarian, Schmidtea mediterranea (Platyhelminthes: Dugesiidae). Environ Sci Pollut Res 26:11326–11335. https://doi.org/10.1007/s11356-019-04532-4
Olson JR (2019) Predicting combined effects of land use and climate change on river and stream salinity. Philos Trans R Soc B 374:1–8. https://doi.org/10.1098/rstb.2018.0005
Pal S, Chakraborty K (2017) Different aspects of chloride in freshwater: a review. Inter J Curr Trends Sci Tech 7:20295–20303
Pedrosa JAM, Cocchiararo B, Bordalo MD, Rodrigues ACM, Soares AMVM, Barata C, Nowak C, Pestana JLT (2017) The role of genetic diversity and past-history selection pressures in the susceptibility of Chironomus riparius populations to environmental stress. Sci Total Environ 576:807–816. https://doi.org/10.1016/j.scitotenv.2016.10.100
Péry AR, Mons R, Flammarion P, Lagadic L, Garric J (2002) A modeling approach to link food availability, growth, emergence, and reproduction forthe midge Chironomus riparius. Environ Toxicol Chem 21:2507–2513. https://doi.org/10.1002/etc.5620211133
Przhiboro A (2014) Diversity and adaptations of immature Diptera in semiaquatic habitats at shorelines of hypersaline lakes in the Crimea, with a brief review of Diptera in mineralized bodies of water. Acta Geol Sin-Engl 88:98–100. https://doi.org/10.1111/1755-6724.12266_22
Reddien PW, Alvarado AS (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20:725–757. https://doi.org/10.1146/annurev.cellbio.20.010403.095114
Rind K, Beyrend D, Charmantier G, Cucchi P, Lignot J (2017) Effects of different salinities on the osmoregulatory capacity of Mediterranean sticklebacks living in freshwater. J Zool 303:270–280. https://doi.org/10.1111/jzo.12491
Riveira VR, Perich MJ (1994) Effects of water quality on survival and reproduction of four species of planaria (Turbellaria: Tricladida). Invertebr Reprod Dev 25:1–7. https://doi.org/10.1080/07924259.1994.9672362
Rodrigues ACM, Gravato C, Quintaneiro C, Golovko O, Žlábek V, Barata C, Soares AMVM, Pestana JLT (2015) Life history and biochemical effects of chlorantraniliprole on Chironomus riparius. Sci Total Environ 508:506–513. https://doi.org/10.1016/j.scitotenv.2014.12.021
Santos MAPF, Vicensotti J, Monteiro RTR (2007) Sensitivity of Four Test Organisms (Chironomus xanthus, Daphnia magna, Hydra attenuata and Pseudokirchneriella subcapitata) to NaCl: an Alternative Reference Toxicant. J Braz Soc Ecotoxicol 2:229–236. https://doi.org/10.5132/jbse.2007.03.004
Santos B, Ribeiro R, Domingues I, Pereira R, Soares AMVM, Lopes I (2013) Salinity and copper interactive effects on perez’s frog Pelophylax perezi. Environ Toxicol Chem 32:1864–1872. https://doi.org/10.1002/etc.2257
Saraiva AS, Sarmento RA, Golovko O, Randak T, Pestana JLT, Soares AMVM (2018) Lethal and sub-lethal effects of cyproconazole on freshwater organisms: a case study with Chironomus riparius and Dugesia tigrina. Environ Sci Pollut Res Int 25:12169–12176. https://doi.org/10.1007/s11356-017-1180-y
Schuler MS, Cañedo-Argüelles M, Hintz WD, Dyack B, Birk S, Relyea RA (2019) Regulations are needed to protect freshwater ecosystems from salinization. Philos Trans R Soc B 374:1–9. https://doi.org/10.1098/rstb.2018.0019
Shadrin NV, Anufriieva EV, Belyakov VP, Bazhora AI (2017) Chironomidae larvae in hypersaline waters of the Crimea: diversity, distribution, abundance and production. Eur Zool J 84:61–72. https://doi.org/10.1080/11250003.2016.1273974
Shadrin NV, Belyakov VP, Bazhora AI, Anufriieva EV (2019a) Does salinity affect body proportions and “size/mass” ratios of highly halotolerant Baeotendipes noctivagus larvae (Diptera, Chironomidae)? Oceanol Hydrobiol Stud 48:305–315. https://doi.org/10.2478/ohs-2019-0028
Shadrin NV, Belyakov VP, Bazhora AI, Anufriieva EV (2019b) The role of salinity as an environmental filtering factor in the determination of the Diptera taxonomic composition in the Crimean waters. Knowl Manag Aquat Ecosyst 420:1–7. https://doi.org/10.1051/kmae/2018041
Soucek DJ, Kennedy AJ (2005) Effects of hardness, chloride, and acclimation on the acute toxicity of sulfate to freshwater invertebrates. Environ Toxicol Chem 24:1204–1210. https://doi.org/10.1897/04-142.1
Sprague JB, Fogels A (1977) Watch the Yin bioassay. Proceedings of the 3rd aquatic toxicity workshop, Halifax, Nova Scotia Nov. 2–3, 1976 Environment Canada, Tech. Report No. EPS-5AR-77-1; p. 107–18
Taenzler V, Bruns E, Dorgerloh M, Pfeifle V, Weltje L (2007) Chironomids: suitable test organisms for risk assessment investigations on the potential endocrine disrupting properties of pesticides. Ecotoxicol 16:221–230. https://doi.org/10.1007/s10646-006-0117-x
Talbot J, Schotz EM (2011) Quantitative characterization of planarian wild-type behavior as a platform for screening locomotion phenotypes. J Exp Biol 214:1063–1067. https://doi.org/10.1242/jeb.052290
Thorp JH, Rogers DC (eds) (2015) Ecology and General Biology. Thorp and Covich’s Freshwater Invertebrates. Vol. 1. 4th ed. Academic Press, Elsevier, Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo
Todd AK, Kaltenecker MG (2012) Warm season chloride concentrations in stream habitats of freshwater mussel species at risk. Environ Pollut 171:199–206. https://doi.org/10.1016/j.envpol.2012.07.040
Tyree M, Clay N, Polaskey S, Entrekin S (2016) Salt in our streams: even small sodium additions can have negative effects on detritivores. Hydrobiologia 775:109–122. https://doi.org/10.1007/s10750-016-2718-6
USEPA - Environmental Protection Agency (1988) Ambient water quality criteria for chloride, EPA-440-5-88-001. Office of Water, Washington, DC
Venâncio C, Castro BB, Ribeiro R, Antunes SC, Abrantes N, Soares AMVM, Lopes I (2019) Sensitivity of freshwater species under single and multigenerational exposure to seawater intrusion. Philos Trans R Soc B 374:1–13. https://doi.org/10.1098/rstb.2018.0252
Venâncio C, Ribeiro R, Lopes I (2020) Active emigration from climate change-caused seawater intrusion into freshwater habitats. Environ Pollut 258:1–19. https://doi.org/10.1016/j.envpol.2019.113805
Vorste RV, Timpano AJ, Cappellin C, Badgley BD, Zipper CE, Schoenholtz SH (2019) Microbial and macroinvertebrate communities, but not leaf decomposition, change along a mining-induced salinity gradient. Freshw Biol 1-14. https://doi.org/10.1111/fwb.13253
Walker I (1987) The biology of streams as part of Amazonian forest ecology. Experientia 43:279–287. https://doi.org/10.1007/BF01945551
Wu JP, Li MH (2018) The use of freshwater planarians in environmental toxicology studies: Advantages and potential. Ecotoxicol Environ Saf 161:45–56. https://doi.org/10.1016/j.ecoenv.2018.05.057
Wu JP, Chen HC, Li MH (2012) Bioaccumulation and toxicodynamics of cadmium to freshwater planarian and the protective effect of N-acetylcysteine. Arch Environ Contam Toxicol 63:220–229. https://doi.org/10.1007/s00244-012-9764-5
Acknowledgments
This study was funded by the National Council for Scientific and Technological Development - CNPq - Brazil (Projects 401201/2014-7 and 200895/2015-0) and the Coordination of Improvement of Higher Education Personnel - CAPES, Brazil (Project PVE - A058_2013). This funding source had no involvement in the experiments, analysis of the data or manuscript preparation. RAS received scholarship from CNPq (Project 306652/2018-8). Thanks are due for the financial support to CESAM (UIDB/50017/2020+UIDP/50017/2020), to FCT/MEC through national funds. The authors also thank FCT and POPH/ FSE (Programa Operacional Potencial Humano/Fundo Social Europeu) for the research contract under the program “Investigador FCT” of JLTP (IF/01420/2015). MDB is funded by national funds (OE), through FCT – Fundação para a Ciência e a Tecnologia, I.P., in the scope of the framework contract foreseen in the numbers 4, 5, and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19.
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Dornelas, A.S.P., Sarmento, R.A., Cavallini, G.S. et al. Lethal and sublethal effects of the saline stressor sodium chloride on Chironomus xanthus and Girardia tigrina. Environ Sci Pollut Res 27, 34223–34233 (2020). https://doi.org/10.1007/s11356-020-09556-9
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DOI: https://doi.org/10.1007/s11356-020-09556-9