Evaluation of the South American gastropod Heleobia parchappii as test organism in cadmium toxicity bioassays

Cecilia L. Achiorno; Graciela Minardi; Marcela I. Schneider; Marilina Fogel

doi:10.25260/EA.23.33.1.0.2058

Authors

Cecilia L. Achiorno Centro de Estudios Parasitológicos y de Vectores (CEPAVE), CCT La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina
Graciela Minardi Centro de Estudios Parasitológicos y de Vectores (CEPAVE), CCT La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina https://orcid.org/0000-0002-7828-2373
Marcela I. Schneider Centro de Estudios Parasitológicos y de Vectores (CEPAVE), CCT La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina https://orcid.org/0000-0001-5666-7742
Marilina Fogel Centro de Estudios Parasitológicos y de Vectores (CEPAVE), CCT La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina https://orcid.org/0000-0001-5911-182X

DOI:

https://doi.org/10.25260/EA.23.33.1.0.2058

Keywords:

mollusk, native species, bioassay, freshwater, acute toxicity, cadmium chloride

Abstract

Gastropods are abundant key components in freshwater ecosystems, many of which are affected by anthropogenic activities. The genus Heleobia is widely distributed across Argentina, and the native Heleobia parchappii is very common in the Pampean Region. The identification of native candidate species for toxicity testing is gaining increasing interest. The objectives of the present study were to evaluate 1) the susceptibility of H. parchappii to a reference toxicant (Cl2Cd), and 2) its suitability for toxicity testing by estimating LC₅₀. Also, we discussed the applicability of the proposed protocol. Snail sensitivity was assessed by exposure to concentrations between 0.5 and 12 mg Cd/L under acute static conditions during 72 h (exposure period). Then, snails were transferred to the control medium for 24 h (post-exposure period) and checked for recovery and those not responding to stimulation were considered to be dead. The endpoints were snail immobilization (recorded every 24 h during the exposure period) and mortality at the end of the post-exposure period. Snail sensitivity was analyzed with a generalized linear mixed model (GLMM) and LC50 (lethal concentration 50%) was calculated using probit analysis. Results indicated that the number of immobilized snails increased with increasing concentration. The toxic effect of Cd on snails persisted 24 h after exposure. The LC₅₀ was 2.145 (1.675-2.641) mg Cd/L. The sensitivity of H. parchappii was similar to that reported for other freshwater standard species, supporting its suitability as test organism. The protocol was appropriate for use in toxicity testing as it is simple, inexpensive and reproducible.

References

Achiorno, C., C. De Villalobos, and L. Ferrari. 2010. Validation test with embryonic and larval stages of Chordodes nobilii (Gordiida, Nematomorpha): Sensitivity to three reference toxicants. Chemosphere 81:133-140. https://doi.org/10.1016/j.chemosphere.2010.06.076.

Albariño, R., A. Venturino, C. M. Montagna, and A. M. Pechen De D’Angelo. 2007. Environmental effect assessment of Magnacide® h herbicide at río Colorado irrigation channels (Argentina). Tier 4: in situ survey on benthic invertebrates. Environmental Toxicology and Chemistry 26:183-189. https://doi.org/10.1897/06-086r.1.

Ansaldo, M., D. E. Nahabedian, C. Di Fonzo, and E. A. Wider. 2009. Effect of cadmium, lead and arsenic on the oviposition, hatching and embryonic survival of Biomphalaria glabrata. Science of The Total Environment 407:1923-192. https://doi.org/10.1016/j.scitotenv.2008.12.001.

Baroudi, F., J. Al Alam, Z. Fajloun, and M. Millet. 2020. Snail as sentinel organism for monitoring the environmental pollution; a review. Ecological Indicators 113:106240. https://doi.org/10.1016/j.ecolind.2020.106240.

Bollani, S., L. De Cabo, C. Chagas, C. Weigandt, A. Fabrizio De Iorio, and A. Magdaleno. 2018. Genotoxicity of water samples from an area of the Pampean Region (Argentina) impacted by agricultural and livestock activities. Environmental Science and Pollution Research 26:27631-27639. https://doi.org/10.1007/s11356-018-3263-9.

Cazzaniga, N. J. 2011a. 1. Heleobia Stimpson, 1865: Taxonomía. Pp. 26-28 in N. J. Cazzaniga (ed.). El género Heleobia (Caenogastropoda: Cochliopidae) en América del Sur. The genus Heleobia (Caenogastropoda: Cochliopidae) in South America. Capítulo colectivo. Amici Molluscarum. Número especial.

Cazzaniga, N. J. 2011b. 6. Notas autoecológicas sobre Heleobia parchappii. Pp. 26-28 in N. J. Cazzaniga (ed.). El género Heleobia (Caenogastropoda: Cochliopidae) en América del Sur. The genus Heleobia (Caenogastropoda: Cochliopidae) in South America. Capítulo colectivo. Amici Molluscarum. Número especial.

Charry, M. P., G. L. Northcott, S. Gaw, V. Keesing, M. J. Costello, and L. A. Tremblay. 2019. Development of acute and chronic toxicity bioassays using the pelagic copepod Gladioferens pectinatus. Ecotoxicology and Environmental Safety 174:611-617. https://doi.org/10.1016/j.ecoenv.2019.03.022.

Chi, H. 2008. TWOSEX-MSChart: Computer program for age-stage, two-sex life table analysis. URL: 140.120.197.183/Ecology.

Chouikhi, A. 1979. Choice and set up of the food chains in freshwater in order to show the bioaccumulation character of a pollutant. In OECD-IRCHA Universite Paris-Sud, Unite d'Enseignement et de Recherche d'Hygiene et Protection de l’Homme et de son Environnement (FRE).

Coeurdassier, M., A. Vaufleury, R. Scheifler, E. Morhain, and P. M. Badot. 2004. Effects of cadmium on the survival of three lifestages of the freshwater pulmonate Lymnaea stagnalis (Mollusca: Gastropoda). Bulletin of Environmental Contamination and Toxicology 72:1083-1090. https://doi.org/10.1007/s00128-004-0354-8.

Dhara, K., N. C. Saha, and A. K. Maiti. 2017. Studies on acute and chronic toxicity of cadmium to freshwater snail Lymnaea acuminata (Lamarck) with special reference to behavioral and hematological changes. Environmental Science and Pollution Research 24:27326-27333. https://doi.org/10.1007/s11356-017-0349-8.

de Freitas Tallarico, L. 2015. Freshwater Gastropods as a Tool for Ecotoxicology Assessments in Latin America. American Malacological Bulletin 33:330-336. https://doi.org/10.4003/006.033.0220.

Drago, F. 2004. Dinámica estacional y ecología de las poblaciones de parásitos del pejerrey, Odontesthes bonariensis (Cuvier and Valenciennes 1835), en lagunas de la provincia de Buenos Aires. Tesis Doctoral. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata.

Fox, J. 2016. Applied Regression Analysis and Generalized Linear Models. 3rd Edition. Chapters 15 (Pp. 418-473), 23 (Pp. 700-742) and 24 (Pp. 743-758). Los Angeles: SAGE Publications Inc.

Gadkari, A. S., and V. B. Marathe. 1983. Toxicity of cadmium and lead to a fish and a snail from two different habitats. Indian Association Water Pollution Control Technology 5:141-148.

Gelman, A., and J. Hill. 2006. Data Analysis Using Regression and Multilevel/Hierarchical Models. Chapters 5 (Pp. 79-108) and 14 (Pp. 301-324). New York: Cambridge University Press.

Giusto, A., L. A. Somma, and L. Ferrari. 2012. Cadmium toxicity assessment in juveniles of the Austral South America amphipod Hyalella curvispina. Ecotoxicology and Environmental Safety 79:163-169. https://doi.org/10.1016/j.ecoenv.2011.12.020.

Giusto, A., A. Salibián, and L. Ferrari. 2014. Cadmium toxicity assessment in juveniles of the Austral South America amphipod Hyalella curvispina. Ecotoxicology 23:163-169. https://doi.org/10.1007/s10646-013-1173-7.

Gómez, N., M. V. Sierra, A. Cortelezzi, and A. Rodrigues Capítulo. 2008. Effects of discharges from the textile industry on the biotic integrity of benthic assemblages. Ecotoxicology and Environmental Safety 69:472-479. https://doi.org/10.1016/j.ecoenv.2007.03.007.

González Sagrario, M. A., D. Rodríguez Golpe, L. La Sala, G. Sánchez Vuichard, P. Minotti, and H. O. Panarello. 2018. Lake size, macrophytes, and omnivory contribute to food web linkage in temperate shallow eutrophic lakes. Hydrobiologia 818:87-103. https://doi.org/10.1007/s10750-018-3594-z.

Gopalakrishnan, S., H. Thilagam, and P. Vivek Raja. 2008. Comparison of heavy metal toxicity in life stages (spermiotoxicity, egg toxicity, embryotoxicity and larval toxicity) of Hydroides elegans. Chemosphere 71:515-528. https://doi.org/10.1016/ j.chemosphere.2007.09.062.

Kammenga, J. E., C. A. M Van Gestel, and J. Bakker. 1994. Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Archives of Environmental Contamination and Toxicology 27:88-94. https://doi.org/10.1007/BF00203892.

Keller, A. E., and S. G. Zam. 1991. The acute toxicity of selected metals to the freshwater mussel, Anodonta imbecilis. Environmental Toxicology and Chemistry: An International Journal 10(4):539-546. https://doi.org/10.1002/etc.5620100415.

Lam, P. K. S. 1996. Interpopulation differences in acute response of Brotia hainanensis (Gastropoda, Prosobranchia) to cadmium: Genetic or environmental variance? Environmental Pollution 94:1-7. https://doi.org/10.1016/s0269-7491(96)00112-1.

Marchese, M. R., A. M. Gagneten, L. Montalto, L. I. Gallardo, M. P. Damborsky, and A. S. G. Poi. 2020. Aplicación de indicadores biológicos en el nordeste argentino. Pp. 99-122 in E. Domínguez, A. Giorgi and N. Gómez (comps.). La bioindicación en el monitoreo y evaluación de los sistemas fluviales de la Argentina: bases para el análisis de la integridad ecológica. 1a ed. Ciudad Autónoma de Buenos Aires: Eudeba. Libro digital. ISBN 978-950-23-3006-8.

Martin, I. G. L., and E. C. Cabrera. 2018. Morphological Characterization of Emerging Cercariae among Lymnaeid Snails from Barangay Cawongan, Padre Garcia, Batangas, Philippines. Journal of Parasitology Research 2018:1-13. https://doi.org/10.1155/2018/5241217.

Merlo, M. J., M. Parietti, and J. A. Etchegoin. 2019.Temporal variations of larval digenean assemblages parasitizing Heleobia parchappii (Mollusca: Cochliopidae) in two shallow lakes from the Buenos Aires province, Argentina. Iheringia, Serie Zoología 109:2019025. https://doi.org/10.1590/1678-4766e2019025.

Oliveira-Filho, E. C., E. Nakano, and L. Tallarico. 2017. Bioassays with freshwater snails Biomphalaria sp.: from control of hosts in public health to alternative tools in ecotoxicology. Invertebrate Reproduction and Development 61:49-57. https://doi.org/10.1080/07924259.2016.1276484.

Piva, F., F. Ciaprini, F. Onorati, M. Benedetti, D. Fattorini, A. Ausili, and F. Regoli. 2011. Assessing sediment hazard through a weight of evidence approach with bioindicator organisms: A practical model to elaborate data from sediment chemistry, bioavailability, biomarkers and ecotoxicological bioassays. Chemosphere 475-485. https://doi.org/10.1016/j.chemosphere.2010.12.064.

R CORE TEAM. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: R-project.org.

Salice, C. J., and T. J. Miller. 2003. Population-level responses to long term cadmium exposure in two strains of a freshwater gastropod Biomphalaria glabrata: Result from a life-table response experiment. Environmental Toxicology Chemistry 22:678-688. https://doi.org/10.1002/etc.5620220329.

Schipper, C. A., I. M. C. Rietjens, R. M. Burgess, and A. J. Murk. 2010. Application of bioassays in toxicological hazard, risk and impact assessments of dredged sediments. Marine Pollution Bulletin 60:2026-2042. https://doi.org/10.1016/j.marpolbul.2010.07.018.

Silva, J., C. Fuentealba, E. Bay-Schmith, and A. Larrain. 2007. Estandarización del bioensayo de toxicidad aguad con Diplodon chilensis usando un toxico de referencia. Gayana (Concepción) [online] 71:135-141. https://doi.org/10.4067/S0717-65382007000200001.

Tietze, E., and C. G. De Francesco. 2010. Environmental significance of freshwater mollusks in the Southern Pampas, Argentina: to what detail can local environments be inferred from mollusk composition? Hydrobiologia 641:133-143. https://doi.org/10.1007/s10750-009-0072-7.

Tietze, E. 2011. Distribución de Heleobia parchappii en ambientes dulceacuícolas de la Región Pampeana (Argentina). Distribution of Heleobia parchappii in freshwater environments of the Pampas (Argentina). Amici Molluscarum, número especial 73-75. Sociedad Malacológica de Chile (SMACH).

US Environmental Protection Agency. 1993. In C. I. Weber (ed.). Methods for Measuring the Acute Toxicity of Effluent and Receiving Waters to Freshwater and Marine Organisms. Fourth ed., EPA-600/4-90-027.

Villar, S., N. Kandratavicius, S. Martínez, and P. Muniz. 2015. Single cell gel electrophoresis as a tool to assess genetic damage in Heleobia cf. australis (Mollusca: Gastropoda) as sentinel for industrial and domestic pollution in Montevideo bay (Uruguay). Brazilian Journal of Oceanography [online] 63:347-354. https://doi.org/10.1590/S1679-87592015090906303.

Williams, P. L., and D. B. Dusenbery. 1990. Aquatic toxicity testing using the nematode, Caenorhabditis elegans. Environmental Toxicology and Chemistry 9:1285-1290. https://doi.org/10.1002/etc.5620091007.

Zou, E., and S. Bu. 1994. Acute toxicity of copper, cadmium, and zinc to the water flea, Moina irrasa (Cladocera). Bulletin of Environmental Contamination and Toxicology 52:742-748. https://doi.org/10.1007/BF00195497.