Does environmental pollution affect male reproductive system in naturally exposed vertebrates? A systematic review
Introduction
Population growth, industrial and technological development, and the intense exploitation of natural resources over the years have resulted in a substantial increase in environmental degradation worldwide [[1], [2], [3]]. The environment receives continuously different contaminants derived from anthropic actions, increasing the levels of environmental pollution. Pollutants from urban, industrial, and agricultural activities put ecological health at risk due to contamination and accumulation in wildlife and humans [4,5]. There is substantial evidence that exposure to environmental contaminants promotes oxidative stress, DNA damage, inflammation, and damage in the tissues [[6], [7], [8]]. Thus, the release of toxic substances into the environment, such as toxic metals, organochlorine pesticides (OCPs), and chemicals [9], in addition to high levels of light, noise, and heat, might cause physiological, morphological, and behavioral changes in living beings [10].
Among these changes, the high frequency of reproductive abnormalities in male vertebrates is directly related to the presence of these animals in polluted areas [11]. These abnormalities end up interfering with the functionality and structure of the gonads and induce hormonal and sperm alterations, which can impair the quality and number of offspring [12]. Therefore, some environmental contaminants' deleterious effects on male reproductive organs are of concern, as they may contribute to the population decline of exposed species [[12], [13], [14]].
Experimental laboratory studies have constantly investigated how environmental contaminants affect the male reproductive system and gametes [[15], [16], [17]]. On the other hand, few works have investigated how these contaminants might affect male reproduction in naturally exposed animals [[18], [19], [20]]. Although controlled laboratory studies provide invaluable preliminary information on the effects of environmental stressors, further studies under natural conditions are needed to increase ecological realism for several reasons, such as the bioavailability of toxicants and interaction among several pollutants [21]. Thus, a better understanding of male reproductive dysfunctions in vertebrates caused by contaminants dispersed in the environment could allow us to identify the species and ecosystems most vulnerable to contamination and distinguish the pollutants that pose the greatest threats to the health of wild animals.
A systematic study of specific reproductive harm from pollution can reveal similar patterns across many species and populations in contact with environmental contaminants [22]. In this framework, we aimed to systematically review the effects of exposure of vertebrate animals to polluted environments on their male reproductive functions, seeking to understand how these contaminants can influence animals in nature.
Section snippets
Guiding question
The main question we sought to answer in this systematic review was: “Can vertebrates naturally exposed to polluted environments develop morphological and functional male reproductive damages compared to unexposed animals?”.
Search strategy
Two complementary research strategies to retrieve potentially relevant studies were applied, as follows: (i) primary search in three comprehensive electronic databases (PubMed-Medline, Scopus, and Web of Sciences), and (ii) secondary search through manual screening of the
Studies included
The initial search resulted in 242 articles in PubMed, Web of Science, and Scopus databases. After removing duplicate articles or articles that did not meet the defined criteria, 26 studies were selected (Fig. 1). Another 13 studies were selected through the reference lists. Therefore, 39 studies were considered for this systematic review. The flow diagram summarizing the literature search process is shown in Fig. 1. The list with the references of all studies included is shown in the
Conclusion
This systematic review revealed the harmful effect of environmental pollution on sex hormones, physiology, and morphology of reproductive organs as well as sperm parameters, of naturally exposed vertebrates. The toxic mechanisms involved are the impairment of hormonal signaling and the excessive production of reactive oxygen species. Our findings shed light on the risk of environmental pollution since wild animals are naturally exposed to several contaminants, such as endocrine disruptors,
Disclaimer
The authors declare no conflict of interest.
CRediT authorship contribution statement
Caroline Paula Assunção de Oliveira: search strategy, studies reviewed, Writing – original draft, wrote the manuscript. Alice Arantes Carneiro: Writing – original draft, wrote and revised the manuscript. Luiz Otavio Guimaraes Ervilha: Writing – original draft, wrote and revised the manuscript. Mariana Machado-Neves: Writing – original draft, wrote and revised the manuscript. Ana Cláudia Ferreira Souza: Writing – original draft, wrote and revised the manuscript. Renner Philipe Rodrigues Carvalho:
Declaration of competing interest
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 paper.
Acknowledgments
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (Ph.D. fellowship to R.P.R.C, process number: 88887.509899/2020-00).
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