Elsevier

Environmental Pollution

Volume 286, 1 October 2021, 117470
Environmental Pollution

Systematic review of reptile reproductive toxicology to inform future research directions on endangered or threatened species, such as sea turtles

https://doi.org/10.1016/j.envpol.2021.117470Get rights and content

Highlights

  • Non-threatened species were the most studied in reptile reproductive toxicology.

  • Contaminant effects on reproduction were seen across different taxa.

  • In vitro bioassays can be used for future studies on threatened sea turtle species.

  • Future studies can assess new biomarkers of endocrine disruption for reptiles.

Abstract

Threatened or endangered reptiles, such as sea turtles, are generally understudied within the field of wildlife toxicology, with even fewer studies on how contaminants affect threatened species reproduction. This paper aimed to better inform threatened species conservation by systematically and quantitatively reviewing available research on the reproductive toxicology of all reptiles, threatened and non-threatened. This review found 178 studies that matched our search criteria. These papers were categorized into location conducted, taxa studied, species studied, effects found, and chemicals investigated. The most studied taxa were turtles (n = 87 studies, 49%), alligators/crocodiles (n = 54, 30%), and lizards (n = 37, 21%). Maternal transfer, sex steroid alterations, sex reversal, altered sexual development, developmental abnormalities, and egg contamination were the most common effects found across all reptile taxa, providing guidance for avenues of research into threatened species. Maternal transfer of contaminants was found across all taxa, and taking into account the foraging behavior of sea turtles, could help elucidate differences in maternal transfer seen at nesting beaches. Sex steroid alterations were a common effect found with contaminant exposure, indicating the potential to use sex steroids as biomarkers along with traditional biomarkers such as vitellogenin. Sex reversal through chemical exposure was commonly found among species that exhibit temperature dependent sex determination, indicating the potential for both environmental pollution and climate change to disrupt population dynamics of many reptile species, including sea turtles. Few studies used in vitro, DNA, or molecular methodologies, indicating the need for more research using high-throughput, non-invasive, and cost-effective tools for threatened species research. The prevalence of developmental abnormalities and altered sexual development and function indicates the need to further study how anthropogenic pollutants affect reproductive output in threatened reptiles.

Introduction

Reptiles are a large taxon of ectothermic animals that inhabit the temperate to equatorial regions of the world. Reptiles include taxa such tuataras (Sphenodon punctatus), squamates (lizards, snakes, and relatives), testudines (turtles), and crocodilians (alligators, crocodiles, gharials, and caimans). Many reptile species are under threat from a range of human activities. Common threats to reptile populations include climate change, habitat alteration and loss, incidental bycatch, harvest for sustenance and illegal trade, and anthropogenic pollutants (Gibbons et al., 2000; Todd et al., 2010). Anthropogenic pollutants include persistent organic pollutants (POPs), trace metals, plastic associated compounds, and endocrine disrupting compounds. Chemical pollutants have been found to have a wide range of effects on reptiles, but compared to mammals or fish, our understanding of the impacts of chemical pollutants on reptiles is limited (Gardner and Oberdorster, 2005).

Arguably, the most important aspect of toxicology for any species is how contaminants may affect reproduction, and therefore species survival (Gibbons et al., 2000; Todd et al., 2010). Most reptiles lay eggs, with many species having temperature dependent sex determination, in which the sex of the offspring is determined by the temperature of the nest (Valenzuela and Lance, 2004). As a result, global events, such as climate change, are already exerting pressures on reptile reproduction (Jensen et al., 2018; Todd et al., 2010). Endangered or threatened reptiles, such as sea turtles, already face other pressures that anthropogenic contaminants could exacerbate. For example, sea turtles have long lifespans that may lead to long-term accumulation of contaminants, which could lead to reproductive impairments reducing population recovery.

Many reviews on reptile reproductive toxicology have focused on specific species and/or specific contaminant types (Boggs et al., 2011; Gardner and Oberdorster, 2005; Guillette et al., 2007), and not all contaminants types and taxa are represented equally. However, due to many shared biological processes (e.g. egg production, temperature dependent sex determination), assessing the body of literature across all reptile taxa could help elucidate effect trends, and inform researchers about additional methods that could be used for other species of interest. Additionally, by reviewing the literature of pollutant effects on reptile reproduction, specifically, where the research was done, what species were studied, and what effects were investigated or found, gaps in knowledge can be identified to prioritize future research. This study presents a systematic quantitative literature review of papers that have investigated reproductive toxicology of reptiles, with a view of guiding future research into the impacts of chemical pollutants on the reproduction of threatened sea turtle species.

Section snippets

Search criteria

This review used a systematic quantitative literature search methodology (Pickering and Byrne, 2014) to identify research that investigated the effects of contaminants on reptile reproduction. Using Google Scholar, Web of Science, and Scopus search engines, the literature was searched using the keywords “reptile”, “lizard”, “snake”, “tuatara”, “tortoise”, “turtle”, “crocodile”, “alligator”, “gharial”, and “caiman” in combination (“or”, “and”) with “reproduction”, “contaminants”, “endocrine

Results

A total of 178 papers satisfied the search criteria and were included in this review. Year of publication ranged from 1986 to 2020, with studies increasing over time (Fig. 1). Most studies were conducted within the United States (n = 91 papers, 51% of papers), Canada (n = 12, 7%), Argentina (n = 12, 6%), China (n = 12, 5%) and Mexico (n = 10, 5%; Fig. 2). The taxa that was most studied were testudines (n = 87, 49%) and crocodilians (n = 54, 30%). Squamates were the least studied (n = 37, 21%)

Gaps in research, country of research, and species studied

With 178 papers catalogued, broad trends were identified for the country where studies were conducted/affiliated, species investigated, experiment type (manipulation of field), effects found, and how those effects differ by taxa. Due to the majority (51%) of studies being affiliated with the United States, the most studied species were, understandably, native to the United States. These included American alligators (Alligator mississippiensis), snapping turtles (Chelydra serpentina), pond

Author statement of Credit

Arthur Barraza: Conceptualization, Methodology, Software, Validation, Formal analysis, Investigation, Data curation, Visualization, Writing – original draft, Writing Revisions. Kimberly Finlayson: Conceptualization, Validation, Visualization, Writing Revisions, Supervision. Frederic Leusch: Conceptualization, Validation, Writing Revisions, Supervision, Project administration, Funding acquisition. Jason van de Merwe: Conceptualization, Validation, Writing Revisions, Supervision, Project

Declaration of competing interest

The authors do not have any conflict of interests to report.

Acknowledgements

The authors thank Dr. Catherine Pickering for her guidance with the methodology. Arthur Barraza was supported by the Griffith University Postgraduate Research Scholarship and the Griffith University International Postgraduate Research Scholarship.

References (134)

  • E.J. Calabrese et al.

    The hormesis database: the occurrence of hormetic dose responses in the toxicological literature

    Regul. Toxicol. Pharmacol.

    (2011)
  • E.J. Calabrese et al.

    The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview

    Toxicol. Appl. Pharmacol.

    (2005)
  • J.E. Cañas et al.

    Organochlorine contaminants in eggs: the influence of contaminated nest material

    Chemosphere

    (2002)
  • G. Canesini et al.

    Temperature- vs. estrogen-induced sex determination in Caiman latirostris embryos: both females, but with different expression patterns of key molecules involved in ovarian development

    Gen. Comp. Endocrinol.

    (2018)
  • L. Chen et al.

    Ecological risk assessment of alpha-cypermethrin-treated food ingestion and reproductive toxicity in reptiles

    Ecotoxicol. Environ. Saf.

    (2019)
  • A.A. Cortes-Gomez et al.

    The current situation of inorganic elements in marine turtles: a general review and meta-analysis

    Environ. Pollut.

    (2017)
  • L. Cruze et al.

    Endogenous and exogenous estrogens during embryonic development affect timing of hatch and growth in the American alligator (Alligator mississippiensis)

    Comp. Biochem. Physiol. B Biochem. Mol. Biol.

    (2015)
  • E. De Andrés et al.

    Persistent organic pollutant levels in eggs of leatherback turtles (Dermochelys coriacea) point to a decrease in hatching success

    Chemosphere

    (2016)
  • C. Dyc et al.

    Pollutant exposure in green and hawksbill marine turtles from the Caribbean region

    Reg. Stud. Mar. Sci.

    (2015)
  • K.A. Finlayson et al.

    Towards the development of standardised sea turtle primary cell cultures for toxicity testing

    Ecotoxicol. Environ. Saf.

    (2019)
  • K.A. Finlayson et al.

    Primary green turtle (Chelonia mydas) skin fibroblasts as an in vitro model for assessing genotoxicity and oxidative stress

    Aquat. Toxicol.

    (2019)
  • K.A. Finlayson et al.

    The current state and future directions of marine turtle toxicology research

    Environ. Int.

    (2016)
  • K.A. Finlayson et al.

    Combining analytical and in vitro techniques for comprehensive assessments of chemical exposure and effect in green sea turtles (Chelonia mydas)

    Chemosphere

    (2021)
  • K.A. Finlayson et al.

    Development and application of species-specific cell-based bioassays to assess toxicity in green sea turtles

    Sci. Total Environ.

    (2020)
  • M.M.P.B. Fuentes et al.

    Using a microclimate model to evaluate impacts of climate change on sea turtles

    Ecol. Model.

    (2013)
  • G.H. Galoppo et al.

    Bisphenol A disrupts the temporal pattern of histofunctional changes in the female reproductive tract of Caiman latirostris

    Gen. Comp. Endocrinol.

    (2017)
  • G.H. Galoppo et al.

    Long-term effects of in ovo exposure to an environmentally relevant dose of atrazine on the thyroid gland of Caiman latirostris

    Environ. Res.

    (2020)
  • G. Garcia-Besne et al.

    Comparison of organochlorine pesticides and PCB residues among hawksbill (Eretmochelys imbricata) and green (Chelonia mydas) turtles in the Yucatan Peninsula and their maternal transfer

    Mar. Pollut. Bull.

    (2015)
  • D.H. Gist

    Hormones and the sex ducts and sex accessory structures of reptiles

    (2011)
  • E. Guirlet et al.

    Maternal transfer of chlorinated contaminants in the leatherback turtles, Dermochelys coriacea, nesting in French Guiana

    Chemosphere

    (2010)
  • M.P. Gunderson et al.

    Variation in sex steroids and phallus size in juvenile American alligators (Alligator mississippiensis) collected from 3 sites within the Kissimmee-Everglades drainage in Florida (USA)

    Chemosphere

    (2004)
  • M.P. Gunderson et al.

    Up-regulation of the alligator CYP3A77 gene by toxaphene and dexamethasone and its short term effect on plasma testosterone concentrations

    Aquat. Toxicol.

    (2006)
  • T. Hartung

    From alternative methods to a new toxicology

    Eur. J. Pharm. Biopharm.

    (2011)
  • C.M. Jandegian et al.

    Developmental exposure to bisphenol A (BPA) alters sexual differentiation in painted turtles (Chrysemys picta)

    Gen. Comp. Endocrinol.

    (2015)
  • M.A. Johnson et al.

    Neuroendocrinology of reptilian reproductive behavior

    (2011)
  • N. Kitana et al.

    Gonadotropin and estrogen responses in freshwater turtle (Chrysemys picta) from Cape Cod, Massachusetts

    Gen. Comp. Endocrinol.

    (2006)
  • J. Matthews et al.

    Differential estrogen receptor binding of estrogenic substances: a species comparison

    J. Steroid Biochem. Mol. Biol.

    (2000)
  • K.C. Miranda Filho et al.

    Lactational transfer of PCBs and chlorinated pesticides in pups of southern elephant seals (Mirounga leonina) from Antarctica

    Chemosphere

    (2009)
  • C.M. Murray et al.

    Methyltestosterone alters sex determination in the American alligator (Alligator mississippiensis)

    Gen. Comp. Endocrinol.

    (2016)
  • L.A. Neuman-Lee et al.

    Physiological effects of polybrominated diphenyl ether (PBDE-47) on pregnant gartersnakes and resulting offspring

    Gen. Comp. Endocrinol.

    (2015)
  • F.M. Nilsen et al.

    Examining maternal and environmental transfer of mercury into American alligator eggs

    Ecotoxicol. Environ. Saf.

    (2020)
  • J.J. Pagano et al.

    Assessment of maternal contaminant burden by analysis of snapping turtle eggs

    J. Great Lake. Res.

    (1999)
  • J. Perrault et al.

    Why are hatching and emergence success low? Mercury and selenium concentrations in nesting leatherback sea turtles (Dermochelys coriacea) and their young in Florida

    Mar. Pollut. Bull.

    (2011)
  • J.R. Perrault et al.

    Maternal transfer and sublethal immune system effects of brevetoxin exposure in nesting loggerhead sea turtles (Caretta caretta) from western Florida

    Aquat. Toxicol.

    (2016)
  • M.J. Portelli et al.

    Effect of dichlorodiphenyltrichloroethane on sex determination of the common snapping turtle (Chelydra serpentina serpentina)

    Ecotoxicol. Environ. Saf.

    (1999)
  • Richard Heath Rauschenberger et al.

    Achieving environmentally relevant organochlorine pesticide concentrations in eggs through maternal exposure in Alligator mississippiensis

    Mar. Environ. Res.

    (2004)
  • F. Rey et al.

    Prenatal exposure to pesticides disrupts testicular histoarchitecture and alters testosterone levels in male Caiman latirostris

    Gen. Comp. Endocrinol.

    (2009)
  • J.A. Shelby et al.

    Comparison of reproductive parameters in male yellow-blotched map turtles (Graptemys flavimaculata) from a historically contaminated site and a reference site

    Comp. Biochem. Physiol. C Toxicol. Pharmacol.

    (2001)
  • J.M. Bergeron et al.

    PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination

    Environ. Health Perspect.

    (1994)
  • A. Cardone et al.

    Effects of the aromatase inhibitor Fadrozole on plasma sex steroid secretion, spermatogenesis and epididymis morphology in the lizard, Podarcis sicula

    Mol. Reprod. Dev.

    (2002)
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