Elsevier

Theriogenology

Volume 198, 1 March 2023, Pages 305-316
Theriogenology

Does environmental pollution affect male reproductive system in naturally exposed vertebrates? A systematic review

https://doi.org/10.1016/j.theriogenology.2023.01.004Get rights and content

Highlights

  • Exposure to pollution could compromise the male reproductive functions of wild animals.

  • Studies are concentrated in North America and report EDCs as aquatic pollutants.

  • Exposure to EDCs reduces androgen levels, impairing reproductive organs and spermatogenesis.

  • Toxic metal pollution is associated with oxidative damage to reproductive organs and sperm.

  • Wildlife is important to understanding the effects of pollution on ecosystem health.

Abstract

Due to environmental contamination, the environment constantly receives pollutants from various anthropic actions. These pollutants put ecological health at risk due to contamination and accumulation in living organisms, including wild animals and humans. Exposure can cause physiological, morphological, and behavioral changes in living beings. In this context, laboratory studies have frequently investigated how environmental contaminants affect the male reproductive system and gametes. However, few studies have examined how these contaminants affect male reproduction in naturally exposed animals. To better understand this topic, we conducted a systematic review of the effects of exposing male vertebrate animals to polluted environments on their reproductive functions. After an extensive search using the PubMed/MEDLINE, Scopus, and Web of Science databases, 39 studies met our inclusion criteria and were eligible for this review. This study showed that reproductive damages were frequent in fishes, amphibians, reptiles, birds, and mammals exposed to contaminated environments. Wild animals are exposed mainly to endocrine-disrupting compounds (EDCs), toxic metals, and radiation. Exposure to pollutants causes a reduction in androgen levels, impaired spermatogenesis, morphological damage to reproductive organs, and decreased sperm quality, leading to reduced fertility and population decline. Although several species have been studied, the number of studies is limited for some groups of vertebrates. Wildlife has proven valuable to our understanding of the potential effects of environmental contaminants on human and ecosystem health. Thus, some recommendations for future investigations are provided. This review also creates a baseline for the understanding state of the art in reproductive toxicology studies.

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).

References (149)

  • 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)
  • G.G. Pyle et al.

    Effects of industrial metals on wild fish populations along a metal contamination gradient

    Ecotoxicol Environ Saf

    (2005)
  • L.B. Bjerregaard et al.

    Intersex in wild roach (Rutilus rutilus) from Danish sewage effluent-receiving streams

    Ecotoxicol Environ Saf

    (2006)
  • T.V. McDaniel et al.

    Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture

    Aquat Toxicol

    (2008)
  • S.M. Bugel et al.

    Impaired reproductive health of killifish (Fundulus heteroclitus) inhabiting Newark Bay, NJ, a chronically contaminated estuary

    Aquat Toxicol

    (2010)
  • M.S. Bornman et al.

    Testicular microlithiasis and neoplastic lesions in wild eland (Tragelaphus oryx): possible effects of exposure to environmental pollutants?

    Environ Res

    (2010)
  • P.S. Prado et al.

    Reproductive disruption in lambari Astyanax fasciatus from a Southeastern Brazilian reservoir

    Ecotoxicol Environ Saf

    (2011)
  • G.R. Tetreault et al.

    Intersex and reproductive impairment of wild fish exposed to multiple municipal wastewater discharges

    Aquat Toxicol

    (2011)
  • P.A. Bahamonde et al.

    Whole organism responses and intersex severity in rainbow darter (Etheostoma caeruleum) following exposures to municipal wastewater in the Grand River basin, ON, Canada. Part A

    Aquat Toxicol

    (2015)
  • M.L.M. Fuzzen et al.

    Severe intersex is predictive of poor fertilization success in populations of rainbow darter (Etheostoma caeruleum)

    Aquat Toxicol

    (2015)
  • S. Persson et al.

    Environmental pollutants and alterations in the reproductive system in wild male mink (Neovison vison) from Sweden

    Chemosphere

    (2015)
  • P. Castellanos et al.

    Increased chromatin fragmentation and reduced acrosome integrity in spermatozoa of red deer from lead polluted sites

    Sci Total Environ

    (2015)
  • N. Amri et al.

    Reproductive effects in hybrid sparrow from a polluted area in Tunisia: oxidative damage and altered testicular histomorphology

    Ecotoxicol Environ Saf

    (2016)
  • Y. Yang et al.

    Response of male reproductive function to environmental heavy metal pollution in a free-living passerine bird, Passer montanus

    Sci Total Environ

    (2020)
  • C.-B. Park et al.

    Biomonitoring the effects of urban-stream waters on the health status of pale chub (Zacco platypus): a comparative analysis of biological indexes and biomarker levels

    Ecotoxicol Environ Saf

    (2021)
  • C.J. Martyniuk et al.

    Transcriptome and physiological effects of toxaphene on the liver-gonad reproductive axis in male and female largemouth bass (Micropterus salmoides)

    Comp Biochem Physiol, Part D: Genomics Proteomics

    (2020)
  • M.I. Jyrkama et al.

    The impact of climate change on spatially varying groundwater recharge in the grand river watershed (Ontario)

    J Hydrol

    (2007)
  • Z. Li et al.

    Impacts of future climate change on river discharge based on hydrological inference: a case study of the Grand River Watershed in Ontario, Canada

    Sci Total Environ

    (2016)
  • M.G. Grillakis et al.

    Climate change impact on the hydrology of spencer creek watershed in southern Ontario, Canada

    J Hydrol

    (2011)
  • P.A. Bahamonde et al.

    Molecular signatures in rainbow darter (Etheostoma caeruleum) inhabiting an urbanized river reach receiving wastewater effluents

    Aquat Toxicol

    (2014)
  • L.R. Iwanowicz et al.

    Aroclor 1248 exposure leads to immunomodulation, decreased disease resistance and endocrine disruption in the brown bullhead

    Ameiurus nebulosus. Aquat Toxicol

    (2009)
  • J.H. Han et al.

    Exotic species, Micropterus salmoides, as a key bioindicator influencing the reservoir health and fish community structure

    J Asia Pac Bus

    (2016)
  • H. Zhang et al.

    Cadmium-induced oxidative stress and apoptosis in the testes of frog Rana limnocharis

    Aquat Toxicol

    (2012)
  • C.M. Bridges et al.

    The interactive effects of UV-B and insecticide exposure on tadpole survival, growth and development

    Biol Conserv

    (2003)
  • R.M. Mann et al.

    Amphibians and agricultural chemicals: review of the risks in a complex environment

    Environ Pollut

    (2009)
  • D.A. Crain et al.

    Reptiles as models of contaminant-induced endocrine disruption

    Anim Reprod Sci

    (1998)
  • L. Marsili et al.

    The Italian wall lizard (Podarcis sicula) as a bioindicator of oil field activity

    Sci Total Environ

    (2009)
  • A.D. Barraza et al.

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

    Environ Pollut

    (2021)
  • J.E.G. Smits et al.

    Avian wildlife as sentinels of ecosystem health

    Comp Immunol Microbiol Infect Dis

    (2013)
  • B.S. Halpern et al.

    A global map of human impact on marine ecosystems

    Science

    (2008)
  • I.O. Tekeli et al.

    Levels of metals and organochlorine pesticides in kidney, liver, and muscle tissues of wild boars (Sus scrofa) from hatay province, eastern mediterranean region, Turkey

    Bull Environ Contam Toxicol

    (2021)
  • E.S.E. Mehana et al.

    Biomonitoring of heavy metal pollution using acanthocephalans parasite in ecosystem: an updated overview

    Animals

    (2020)
  • C. Isaksson

    Pollution and its impact on wild animals: a meta-analysis on oxidative stress

    EcoHealth

    (2010)
  • C. Losacco et al.

    Particulate matter air pollution and respiratory impact on humans and animals

    Environ Sci Pollut Res

    (2018)
  • T.M. Edwards et al.

    Reproductive dysgenesis in wildlife: a comparative view

    Int J Androl

    (2006)
  • L. Multigner et al.

    Parallel assessment of male reproductive function in workers and wild rats exposed to pesticides in banana plantations in Guadeloupe

    Environ Health

    (2008)
  • L.C. Aulsebrook et al.

    Reproduction in a polluted world: implications for wildlife

    Reproduction

    (2020)
  • S. Andleeb et al.

    Environmental chromium from the tannery industry induces altered reproductive endpoints in the wild female small Indian mongoose (urva auropunctatus)

    Toxicol Ind Health

    (2019)
  • J.P. Desforges et al.

    Predicting global killer whale population collapse from PCB pollution

    Science

    (2018)
  • K. Van den Belt et al.

    Effects of ethynylestradiol on the reproductive physiology in zebrafish (danio rerio): time dependency and reversibility

    Environ Toxicol Chem

    (2002)
  • Cited by (5)

    View full text