Abstract
Reptiles are the least studied vertebrates regarding the impact of pesticides on their health, despite being good models for ecotoxicological studies given their abundance and easy handling. Salvator merianae is widely distributed in South America and often found in agricultural cultivation areas. Here, we compared the morphological, biochemical, and physiological parameters of S. merianae from an exposed area (EA) to pesticides and a reference area (RA) or control. These parameters were measured in plasma (albumin, alanine transaminase, alkaline phosphatase, gamma-glutamyl transpeptidase, glucose, total proteins, uric acid, triglycerides, VLDL, and corticosterone) and in erythrocytes (TBARS, glutathione S-transferase, superoxide dismutase, and catalase activity). Blood samples were collected from 28 lizards (EA: three juveniles, three adult females, and three adult males; RA: nine juveniles, four females, and five males) in southern Brazil during the reproductive period. We observed a decrease in body mass, the ratio between body mass and total length and snout-vent length in juvenile lizards collected at EA. The levels of TBARS, glutathione S-transferase, triglycerides, VLDL, and uric acid were altered for juveniles in EA. When comparing the two areas, females differed in superoxide dismutase activity and total proteins, while males differed in superoxide dismutase, catalase, and glutathione S-transferase activity. This set of results shows that S. merianae, especially juveniles, suffers a negative impact when inserted in an agricultural area. The analyzed biomarkers proved suitable for monitoring these lizards and the quality of this environment.
Graphical Abstract
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author, [GTO], upon reasonable request.
References
Amaral, M. J., Carretero, M. A., Bicho, R. C., Soares, A. M., & Mann, R. M. (2012a). The use of a lacertid lizard as a model for reptile ecotoxicology studies-Part 1 field demographics and morphology. Chemosphere, 87(7), 757–764. https://doi.org/10.1016/j.chemosphere.2011.12.075
Amaral, M. J., Bicho, R. C., Carretero, M. A., Sanchez-Hernandez, J. C., Faustino, A. M., Soares, A. M., & Mann, R. M. (2012b). The use of a lacertid lizard as a model for reptile ecotoxicology studies: Part 2—biomarkers of exposure and toxicity among pesticide exposed lizards. Chemosphere, 87, 765–774. https://doi.org/10.1016/j.chemosphere.2012.01.048
Araújo, C. C., Pereira, R. L. S. W., & Flynn, M. N. (2011). Fator de condição e relação peso-comprimento de Mugil curema Valenciennes, 1836 (Pisces, Mugilidae) como potencial bioindicador de contaminação por HPAs em ambientes estuarinos. Revista Intertox De Toxicologia, Risco Ambiental E Sociedade, 4(3). https://doi.org/10.22280/revintervol4ed3.94
Arguedas, R., Gómez, A., Barquero, M. D., Chacón, D., Corrales, G., Hernández, S., Artacho, P., Soto-Gamboa, M., Verdugo, C., & Nespolo, R. F. (2007). Blood biochemistry reveals malnutrition in black-necked swans (Cygnus melanocoryphus) living in a conservation priority area. Comparative biochemistry and physiology. Part a, Molecular & Integrative Physiology, 146(2), 283–290. https://doi.org/10.1016/j.cbpa.2006.10.031
Arguedas, R., Gómez, A., Barquero, M. D., Chacón, D., Corrales, G., Hernández, S., & León, G. (2018). Effect of exposure to chlorpyrifos upon plasma cholinesterases, hematology and blood biochemistry values in Bothrops asper (Serpentes: Viperidae). Chemosphere, 205, 209–214. https://doi.org/10.1016/j.chemosphere.2018.04.111
Boveris, A. & Chance, B. (1973). The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochemical Journal, 134(3), 707–716. https://doi.org/10.1042/bj1340707
Boyland, E., & Chasseaud, L. F. (1969). The role of glutathione and glutathione S-transferases in mercapturic acid biosynthesis. Advances in Enzymology and Related Areas of Molecular Biology, 1969(32), 173–219.
Burella, P. M., Odetti, L. M., Simoniello, M. F., & Poletta, G. L. (2018). Oxidative damage and antioxidant defense in Caiman latirostris (Broad-snouted caiman) exposed in ovo to pesticide formulations. Ecotoxicology and Environmental Safety, 161, 437–443. https://doi.org/10.1016/j.ecoenv.2018.06.006
Carvalho, J. E., Zena, L. A., Pereira, I. C., Bícego, K. C., & Navas, C. A. (2020). Variação sazonalda temperature corporal e do metabolismo energético. In K. C. Bícego & L. H. Gargaglioni (Eds.), Fisiologia térmica de vertebrados (pp. 275–299). Cultura Acadêmica.
Coltro, M., et al. (2017). Influence of the herbicide Facet® on corticosterone levels, plasma metabolites, and antioxidant system in the liver and muscle of American bullfrog tadpoles. Water, Air, and Soil Pollution, 228, 241. https://doi.org/10.1007/s11270-017-3404-7
Contador-Kelsall, I., Maute, K., Story, P., Hose, G. C., & French, K. (2022). Sublethal pesticide exposure influences behaviour, but not condition in a widespread Australian lizard. Conservation Physiology, 10(1), 024. https://doi.org/10.1093/conphys/coac024
Contador-Kelsall, I., Maute, K., de Beer, M., et al. (2023). Individual variation within wild populations of an arid-zone lizard dictates oxidative stress levels despite exposure to sublethal pesticides. Ecotoxicology, 32, 470–486. https://doi.org/10.1007/s10646-023-02653-8
da Silva, O. D., da Costa, T. M., Silva-Alves, V. D., Fermiano, E. C., Seba, M. D. F. R., Nogueira, O. M., Mudrek, J. R., Barbosa, A. P. D., Gusmão, A. C., Muniz, C. C., & Carniello, M. A. (2020a). Diet and food ontogeny of the lizard Tupinambis matipu Silva et al. 2018 (Squamata: Teiidae) in Central Brazil. Research, Society and Development, 9(11), e52391110073–e52391110073.
de Castro, B. D., Lanés, L. E. K., Godoy, R. S., Cubas, G. K., Dabdab, A. B., Maltchik, L., & Oliveira, G. T. (2023). Glyphosate-induced biochemical changes in female Cynopoecillus sp. Inhabiting temporary wetlands. Toxicological and Environmental Chemistry, 1, 1–15. https://doi.org/10.1080/02772248.2023.2246614
Donadio, O. E., & Gallardo, J. M. (1984). Biología y conservación de las especies del género Tupinambis (Squamata, Sauria, Teiidae) en la República Argentina. Revista Del Museo Argentino De Ciencias Naturales Bernardino Rivadavia, 13, 117–127.
Doumas, B. T., Watson, W. A., & Biggs, H. G. (1997). Albumin standards and the measurement of serum albumin with bromcresol green. Clinica Chimica Acta, 258(1), 21–30. https://doi.org/10.1016/S0009-8981(96)06447-9
Eisenreich, K. M., & Rowe, C. L. (2013). Experimental exposure of eggs to polybrominated diphenyl ethers BDE-47 and BDE-99 in red-eared sliders (Trachemys scripta elegans) and snapping turtles (Chelydra serpentina) and possible species-specific differences in debromination. Environmental Toxicology and Chemistry, 32(2), 393–400. https://doi.org/10.1002/etc.2061
Freitas, L., Paranaíba, J., Peréz, A., Machado, M., & Lima, F. (2020). Toxicity of pesticides in lizards. Human & Experimental Toxicology., 39(5), 596–604. https://doi.org/10.1177/0960327119899980
Gomiero, L. M., & de Souza Braga. F. M. (2003). Relação peso-comprimento e fator de condição para Cichla cf. ocellaris e Cichla monoculus (Perciformes, Cichlidae) no reservatório de Volta Grande, rio Grande-MG/SP. Acta Scientiarum: Biological Sciences, 79–86, https://doi.org/10.4025/actascibiolsci.v25i1.2119
González, F. H. D., & Silva, S. C. (2006). Introdução à Bioquímica Clínica Veterinária (2ª, p. 358p). Porto Alegre: UFRGS.
Green, A. J. (2001). Mass/length residuals: measures of body condition or generators of spurious results? Ecology, 82(5), 1473–1483. https://doi.org/10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2
Halán, M., Kottferová, L., Račka, K., & Lam, A. (2022). The amount of food ingested and its impact on the level of uric acid in the blood plasma of snakes. Animals (basel)., 12(21), 2959. https://doi.org/10.3390/ani12212959
Halliwell, B. (2012). Free radicals and antioxidants: Updating a personal view. Nutrition Reviews, 70(5), 257–265. https://doi.org/10.1111/j.1753-4887.2012.00476.x
Hatano, T., & Sasa, S. I. (2001). Steady-state thermodynamics of Langevin systems. Physical Review Letters, 86(16), 3463. https://doi.org/10.1103/PhysRevLett.86.3463
Hedge, G., & Krishnamurthy, S. V. (2014). Analysis of health status of the frog Fejervarya limnocharis (Anura: Ranidae) living in rice paddy fields of Western Ghats, using body condition factor and AChE content. Ecotoxicology and Environmental Contamination, 9(1), 69–76. https://doi.org/10.5132/eec.2014.01.009
Innis, C. J., Ravich, J. B., Tlusty, M. F., Hoge, M. S., Wunn, D. S., Boerner-Neville, L. B., Merigo, C., & Weber III, E.S. (2009). Hematologic and plasma biochemical findings in cold-stunned Kemp’s ridley turtles: 176 cases (2001–2005). Journal of the American Veterinary Medical Association, 235 (4). https://doi.org/10.2460/javma.235.4.426
IUCN- International Union for Conservation of Nature and Natural Resources Red List of threatened species (2020) Lizards. The Red List. https://www.iucnredlist.org/search?query=lizards&searchType=species
Jakob, E. M., Marshall, S. D., & Uetz, G. W. (1996). Estimating fitness: a comparison of body condition indices. Oikos, 77(1), 61–67. https://doi.org/10.2307/3545585
Kanbur, M., Liman, B. C., Eraslan, G., & Altinordulu, S. (2008). Effects of cypermethrin, propetamphos, and combination involving cypermethrin and propetamphos on lipid peroxidation in mice. Environmental Toxicology, 23(4), 473–479. https://doi.org/10.1002/tox.20360
Kiefer, M. C., & Sazima, I. (2002). Diet of juvenile tegu lizard Tupinambis merianae (Teiidae) in southeastern Brazil. Amphibia-Reptilia, 23, 105–108.
Le Cren, C. D. (1951). The length-weight relationship and seasonal cycle in Gonad weight and condition in Perch. Perca fluviatilis. Journal of Animal Ecology, 20, 201–219. https://doi.org/10.2307/1540
Lima, E. S., & Abdalla, D. S. P. (2001). Peroxidação lipídica: mecanismos e avaliação em amostras biológicas. Revista Brasileira de Ciências Farmacêuticas, 37(3), 293–303.
Lucas, L. D., & French, S. S. (2012). Stress-induced tradeoffs in a free-living lizard across a variable landscape: consequences for individuals and populations. PLoS ONE, 7(11), e49895. https://doi.org/10.1371/journal.pone.0049895
Marins, A. T., Cerezer, C., Leitemperger, J. W., Severo, E. S., Costa, M. D., Fontoura, D. O., Nunes, M. E. M., Ribeiro, L. C., Zanella, R., & Loro, V. L. (2021). A mixture of pesticides at environmental concentrations induces oxidative stress and cholinergic effects in the neotropical fish Rhamdia quelen. Ecotoxicology, 30(1), 164–174. https://doi.org/10.1007/s10646-020-02300-6
Memon, A. S. (2020). Hepatotoxic effects on subchronic exposure to chlorpyrifos insecticide in Pigeon (Columba livia domestica). Pure and Applied Biology, 9(1), 172–179. https://doi.org/10.19045/bspab.2020.90021
Mestre, A. P., Amavet, P. S., Vanzetti, A. I., Moleón, M. S., ParachúMarcó, M. V., Poletta, G. L., & Siroski, P. A. (2019). Effects of cypermethrin (pyrethroid), glyphosate and chlorpyrifos (organophosphorus) on the endocrine and immune system of Salvator merianae (Argentine tegu). Ecotoxicology and Environmental Safety, 169, 61–67. https://doi.org/10.1016/j.ecoenv.2018.10.057
Meylan, S., Haussy, C., & Voituron, Y. (2010). Physiological actions of corticosterone and its modulation by an immune challenge in reptiles. General and Comparative Endocrinology, 169(2), 158–166. https://doi.org/10.1016/j.ygcen.2010.08.002
Mingo, V., Lötters, S., & Wagner, N. (2017). The impact of land use intensity and associated pesticide applications on fitness and enzymatic activity in reptiles-a field study. The Science of the Total Environment, 590–591, 114–124. https://doi.org/10.1016/j.scitotenv.2017.02.178
Monaghan, P., Metcalfe, N. B., & Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters, 12, 75–92. https://doi.org/10.1111/j.1461-0248.2008.01258.x
Odetti, L. M., et al. (2023). How the exposure to environmentally relevant pesticide formulations affects the expression of stress response genes and its relation to oxidative damage and genotoxicity in Caiman latirostris. Environmental Toxicology and Pharmacology, 97, 104014. https://doi.org/10.1016/j.etap.2022.104014
Oliveira, A. S. (2015). Uso da radiotelemetria no monitoramento de lagartos: estudo de caso em Salvator merianae. Monografia (Especialização), Universidade Federal do Rio Grande do Sul. https://lume.ufrgs.br/bitstream/handle/10183/141993/000987106.pdf?sequence=1&isAllowed=y
Oliveira, M. R., et al. (2018). Seasonal and sexual variation of the intermediate metabolism and body condition indexes in the lizard Tropidurus catalanensis (Gudynas and Skuk, 1983) (Squamata: Tropiduridae). South American Journal of Herpetology, 13, 85–95. https://doi.org/10.2994/SAJH-D-17-00073.1
Oliveira, M. R., et al. (2021). Evaluation of the seasonal variation of parameters of oxidative status of Tropidurus catalanensis Gudynas and Skuk, 1983. South American Journal of Herpetology, 19, 12–21. https://doi.org/10.2994/SAJH-D-18-00048.1
Paz, M. M., García, N. E., Semhan, R. V., et al. (2019). (2019) Study of lipid reserves in Liolaemus koslowskyi (Squamata: Liolaemidae): Reproductive and ecological implications. Journal of Comparative Physiology B, 189, 595–609. https://doi.org/10.1007/s00360-019-01226-8
Poletta, G. L., Simoniello, M. F., & Mudry, M. D. (2016). Biomarkers of oxidative damage and antioxidant defense capacity in Caiman latirostris blood. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 179, 29–36. https://doi.org/10.1016/j.cbpc.2015.08.003
Puerta, M., Abelenda, M., Salvador, A., Martin, J., Lopez, P., & Veiga, J. P. (1996). Haematology and plasma chemistry of male lizards, Psammodromus algirus. Effects of Testosterone Treatment Comparative Haematology International, 6, 102–106. https://doi.org/10.1007/BF00426050
Schaumburg, L. G., et al. (2016). Genotoxicity induced by Roundup® (Glyphosate) in tegu lizard (S. merianae) embryos. Pesticide Biochemistry and Physiology, 130, 71–78. https://doi.org/10.1016/j.pestbp.2015.11.009
Schulte-Hostedde, A. I., Zinner, B., Millar, J. S., & Hickling, G. J. (2005). Restitution of mass-size residuals: Validating body condition indices. Ecology, 86(1), 155–163. https://doi.org/10.1890/04-0232
Settle, T., & Klandorf, H. (2014). The role of uric acid as an antioxidant in selected neurodegenerative disease pathogenesis: a short review. Brain Disord Ther, 3, 129. https://doi.org/10.4172/2168-975X.1000129
Silva, J. M., Navoni, J. A., & Freire, E. M. X. (2020b). Lizards as model organisms to evaluate environmental contamination and biomonitoring. Environmental Monitoring and Assessment, 192, 454. https://doi.org/10.1007/s10661-020-08435-7
Silvestre, A. M., Dominguez, M. A. R., Mateo, J. A., et al. (2004). Comparative haematology and chemistry of endangered lizards (Gallotia species) in the Canary Islands. Veterinary Record., 155, 266–269. https://doi.org/10.1136/vr.155.9.266
Simbula, G., Vignoli, L., & Carretero, M. A. (2021). Kaliontzopoulou A (2021) Fluctuating asymmetry as biomarker of pesticides exposure in the Italian wall lizards (Podarcis siculus). Zoology, 147, Article 125928. https://doi.org/10.1016/j.zool.2021.125928
Spadotto, C. A. (2006). Abordagem interdisciplinar na avaliação ambiental de agrotóxicos. Revista Núcleo de Pesquisa Interdisciplinar. http://www.fan.edu.br/npi_2.php. 9p. Acessado em 10 de maio de 2018
Speakman John, R. (2008). The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society, B363375–398. https://doi.org/10.1098/rstb.2007.2145
Stahl, S. J. (2003). Diseases of the reptile pancreas. Veterinary Clinics of North America: Exotic Animal Practice, 6(1), 191–212. https://doi.org/10.1016/s1094-9194(02)00054-3
Sykes, J. M., & Klaphake, E. (2015). Reptile hematology. Clinics in Laboratory Medicine, 35(3), 661–680.
Thrall, M. A., Weiser, G., Allison, R. W., & Campbell, T. W. (2015). Hematologia e Bioquímica Clínica Veterinária (2ª, p. 688p). São Paulo: Roca.
Viana, D. C., da Silva, K. B., dos Santos, A. C., & Oliveira, A. S. (2014). Perfil bioquímico em serpentes - revisão de literatura. Revista Campo Digital, 9(1). https://revista.grupointegrado.br/revista/index.php/campodigital/article/view/1719
Vieira, R. C., de Oliveira, A. S., Fagundes, N., Jr., & Verrastro, L. (2015). Approaches to capturing the Black and White Tegu S merianae (Squamata: Teiidae). Zoologia (curitiba. Online), 32, 317–320. https://doi.org/10.1590/S1984-46702015000400007
Wang, Z., et al. (2021). Effects of simazine and food deprivation chronic stress on energy allocation among the costly physiological processes of male lizards (Eremias argus). Environmental Pollution, 269, 116139. https://doi.org/10.1016/j.envpol.2020.116139
Wilkens, A. L. L., Valgas, A. A. N., & Oliveira, G. T. (2019). Effects of ecologically relevant concentrations of Boral® 500 SC, Glifosato® Biocarb, and a blend of both herbicides on markers of metabolism, stress, and nutritional condition factors in bullfrog tadpoles. Environmental Science and Pollution Research International, 26(23), 23242–23256. https://doi.org/10.1007/s11356-019-05533-z
Winck, G. R. (2007). História natural de Tupinambis merianae (Squamata, Teiidae) na Estação Ecológica do Taim, extremo sul do Brasil. Universidade Federal de Santa Maria.
Zena, L. A., Dillon, D., Hunt, K. E., Navas, C. A., Bícego, K. C., & Buck, C. L. (2019). Seasonal changes in plasma concentrations of the thyroid, glucocorticoid and reproductive hormones in the tegu lizard Salvator merianae. General and Comparative Endocrinology, 273, 134–143. https://doi.org/10.1016/j.ygcen.2018.06.006
Acknowledgements
We thank the National Council for Scientific and Technological Development-CNPq for the scholarship granted to the first author and Fundação Empresa Escola de Engenharia (FEEng) for the funds to purchase kits for analyses.
Funding
Partial financial support was received from the National Council for Scientific and Technological Development-CNPq and the Fundação Empresa Escola de Engenharia (FEEng).
Author information
Authors and Affiliations
Contributions
Jéssica Fonseca Araujo: conceptualization, data curation, formal analysis, investigation, writing the manuscript draft. Artur Antunes Navarro Valgas: collection, data curation, review of the manuscript. Diogo Reis de Oliveira: collection, review of the manuscript. Laura Verrastro: conceptualization, formal analysis, methodology, supervision, reviewing, and editing the manuscript. Guendalina Turcato Oliveira: conceptualization, formal analysis, methodology, supervision, writing, reviewing, and editing the manuscript.
Corresponding author
Ethics declarations
Ethics approval
All authors have read, understood, and have complied as applicable with the statement on “Ethical responsibilities of Authors” as found in the Instructions for Authors. The project was carried out after obtaining licenses for handling live animals and blood collection by the Chico Mendes Institute for Biodiversity Conservation (ICMBio), under registration 66925–1, and by the Ethics Commission for the use of Animals at the PUCRS. The access record of genetic heritage was obtained from the National System for the Management of Genetic Heritage and Associated Traditional Knowledge (SISGEN: A4036FB).
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Araujo, J.F., Valgas, A.A.N., de Oliveira, D.R. et al. Pesticides compromise health: a comparison between lizards collected within and outside an agricultural area. Environ Monit Assess 196, 334 (2024). https://doi.org/10.1007/s10661-024-12498-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-024-12498-1