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