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Stress Response, Immunity, and Organ Mass in Toads (Rhinella diptycha) Living in Metal-Contaminated Areas

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Abstract

Mining is one of the main activities that drive the economy of Brazil. Mining activity is associated with risk of contamination of environment and local fauna by metals. Amphibians have a life cycle that requires a transition between aquatic and terrestrial environments, increasing their vulnerability to metal contamination in the water and substrate. Metals are ubiquitous, with high bioaccumulative and biomagnifying potential, and may lead to immune and endocrine disruption. In this study, we analyzed two different components of the innate immune response, bacterial killing ability (BKA) and phytohemagglutinin edema (PHA), and two stress biomarkers, corticosterone plasma levels (CORT) and the neutrophil to lymphocyte ratio (N:L), of toads (Rhinella diptycha) living in places contaminated by metals. Blood samples were collected pre- and post-restraint (1h), followed by an immune challenge with PHA and tissue collection (liver, spleen, and kidneys). Toads liver metal bioaccumulation did not correlate with the immune response or stress biomarkers. Post-restraint, animals had increased CORT and reduced BKA, independently of the collection site, and these variables were not correlated with liver metal bioaccumulation. Interestingly, toads with the larger spleen (immune organ) showed increased N:L post-restraint and greater edema after the PHA challenge. Our results indicate that toads living in metal-contaminated environments responded to acute stressor, activating the hypothalamic-pituitary-interrenal axis and the immune response. Keep tracking the physiological variables of these animals and the presence of metals in the environment and tissues should provide valuable health status indicators for the population, which is vital for proposing amphibian conservation strategies in these areas.

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Data Availability

The original data used in this manuscript will be available at the Mendeley Data, through the DOI: 10.17632/xmygd6msg8.1.

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Acknowledgements

The authors thank the technicians Márcio P. Lima and Raphaela C. Ribeiro for field support; Sheila C. Silva and Rayssa L. Cardoso for support in biochemistry analyses; and Prof. Jorge A. S. Tenório and the lab technician, Ana C. F. Dalsin, for support on metal analyses.

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Funding

This work was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (institutional quota) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (grant number: 2014/16320-7). F.R. Gomes is a research fellow from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—#302308/2016-4.

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Authors and Affiliations

  1. Laboratory of Behavior and Evolutionary Physiology, lab. 206, Department of Physiology, Institute of Biosciences, University of São Paulo, São Paulo, Brazil

    Ronyelle Vasconcelos-Teixeira, Stefanny C. M. Titon, Fernando R. Gomes & Vania R. Assis

  2. Laboratory of Disease & Drug-Associated Receptors Knowledge, Department of Physiology, Institute of Biosciences, University of São Paulo, São Paulo, Brazil

    Stefanny C. M. Titon

  3. Laboratory of Ecophysiology and Evolutionary Physiology, Department of Physiology, Institute of Biosciences, University of São Paulo, São Paulo, Brazil

    Braz Titon Jr

  4. Laboratory of Limnology, Department of Ecology, Institute of Biosciences, University of São Paulo, São Paulo, Brazil

    Marcelo L. M. Pompêo

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Vasconcelos-Teixeira: conceptualization, methodology, validation, formal analysis, investigation, data curation, writing—original draft and editing, visualization, and project administration. Titon: methodology, validation, formal analysis, investigation, and writing—review and editing. Titon Jr: formal analysis, data curation, and writing—review and editing. Pompeo: methodology, resources, and writing—review and editing. Gomes: resources, writing—review and editing, supervision, and funding acquisition. Assis: conceptualization, methodology, writing—review and editing, visualization, and supervision.

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Correspondence to Ronyelle Vasconcelos-Teixeira.

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The collection of the specimens was approved by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, process 29896-1). The ethical approval for the experiments with the animals was granted by the Ethics Committee on Animal Use of the Bioscience Institute of the University of Sao Paulo (CEUA n° 303/2017).

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Vasconcelos-Teixeira, R., Titon, S.C.M., Titon, B. et al. Stress Response, Immunity, and Organ Mass in Toads (Rhinella diptycha) Living in Metal-Contaminated Areas. Biol Trace Elem Res 200, 800–811 (2022). https://doi.org/10.1007/s12011-021-02699-x

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