Effects of ecosystem stress on reproduction and development

During the past decades, vast quantities of different contaminants have been released into terrestrial and marine environments due to land erosion, industrial, agricultural, urban, technological applications, and other anthropogenic activities. Most of the substances known as xenobiotics include metals, pesticides, herbicides, antifouling compounds, nanoparticles, and plastics (Gogoi et al., 2018). However, the environment is threatened not only by chemical insults but also by climate changes, which includes global warming and ocean acidification. Either chemical pollution and climatic modifications are creating a raising alarm in the scientific community and governments due to the potential toxic, genotoxic and carcinogenic impact on living organisms and humans. A large body of evidence indicates that chemical pollution interferes with hormone function giving rise to the so-called endocrine disruption. Due to the vulnerability of hormone-receptor systems, it appears that some endocrine disruptors (EDs) affect the normal reproductive functions and embryo development. Perturbation of wildlife hormonal pathways generate reproductive failures and abnormalities in the reproductive organs of fish, birds, reptiles, and mammals (Colborn, Dumanoski, Myers, & Murden, 1996; Danzo, 1997; Sharpe & Skakkebaek, 1993). It has been demonstrated that reproductive impacts of EDs are due to different mechanisms as mimicking or antagonizing hormonal effects, pattern alteration of hormones synthesis, and metabolism and modification of hormone–receptor interaction (Grindler et al., 2018; Soto et al., 1995). These perturbations may seriously impact male and female gonadal development and, in humans in particular, clinical evidence and epidemiological studies have highlighted an association between EDs action and reproduction disorders, such as gametogenesis and gamete quality impairment, fertility rate decrease, endometriosis (Sifakis, Androutsopoulos, Tsatsakis, & Spandidos, 2017) as well as testicular and ovarian cancers (Maqbool, Mostafalou, Bahadar, & Abdollahi, 2016). Bisphenol A (BPA) is an ED, which is present globally because it is widely used in food and storage containers and beverage bottles also for infant feeding. A recent source of concern is the associations between BPA exposure and reproductive disorders. Literature from the last decades reports that BPA is a reproductive toxicant impacting male and female reproductive systems in humans and animals ultimately threatening fitness and health (Tomza-Marciniak, Stępkowska, Kuba, & Pilarczyk, 2018). Following epidemiological studies, some of the EDs have been banned from the commerce due to their adverse effects on human health and the environment. Among them, organotins, fully utilized as biocides in antifouling paints, have shown to induce imposex a warring reproductive disorder, which induce the overlap of male genitalia in the female of marine gastropods (Horiguchi, 2006). Nonetheless a decade of international prohibition to be used, organotins persist in the environment because of their accumulation in sediments and subsequent release in the water body. A number of experimental studies reinforce the concept that antifouling substances of old and new generation have detrimental effects on the reproductive and developmental mechanisms of marine species (Gallo & Tosti, 2013, 2015) highlighting the risk for species extinction and for transmitting chemical contamination to seafood consumers (Mattos et al., 2017). Metals are the most common pollutants, and although some of them are essential for physiological functions, they become toxic at high concentration and together with nonessential metals exert adverse effects on either animal and human reproductive functions (Gallo, Silvestre, Cuomo, Papoff, & Tosti, 2011; Wirth & Mijal, 2010). The use of engineered nanomaterials in industry, consumer products, and biomedicine is rapidly expanding giving rise to socioeconomic advantages but posing at risk environment and its biota for the high toxicity related to nanoparticles release and persistence in water, air, and soil. By using animal models, a large body of studies are evaluating the effects of several nanoparticles on human health and the reproductive systems of both male and female. These are clearly demonstrating different impacts of nanoparticles on reproductive organs ad systems structure, function, and physiology and the generation of adverse effects on germ cells and in turn on fertility potential. In pregnant women, a peculiar concern arises, the fetotoxic impact due to the easy penetration of small particles through the defensive placental barrier (Brohi et al., 2017). In our experience, two nanoparticles widely used in manufacturing products as nickel and copper oxide exert spermiotoxic impact in two different marine invertebrates. In particular, we demonstrated an adverse effect on some parameters underlying sperm function as concentration, motility, morphology, mitochondrial potential, and the generation of oxidative stress which in turn affected the membrane and genome integrity (Gallo, Boni, Buttino, & Tosti, 2016; Gallo et al., 2018; Rotini et al., 2018). This sperm quality impairment resulted in an impairment of the fertilizing ability in both the species supporting the current concern for fertility reduction of marine species and the potential implications on reproductive fitness and survival of the aquatic biota. Plastics are considered environmental contaminants of emerging concern (Law, 2017). They are constituents of several manufactures as bottles, shopping bags, paints and cosmetics, furthermore they are used for biomedical applications in drug delivery. The increase of plastic production over the last 60 years has led to the estimation that they will persist in in many habitats (PlasticsEurope, 2015) from 10 to 100 years, therefore plastic and their derivate are defined as persistent organic pollutants. In the environment, plastic is known to deteriorate and fragment occurring in different sizes, according to which it is classified in macro- (≥1 cm), meso- (1–10 mm), micro- (1–1000 μm) and nanoplastics (1–1000 nm). In a water body, microplastic due to the small size are able to penetrate in the tissues affecting physiology of living organisms, inducing pathologies from inflammation to tumor development and exerting also serious impact on the reproductive processes of animals and human (Auta, Emenike, & Fauziah, 2017). Polystyrene is among the most diffused nanoplastic in the oceans. The effects of different sizes were evaluated on some reproductive steps as fertilization, embryogenesis and metamorphosis of marine molluscs showing a significant decrease in fertilization rate and in embryo–larval development ranging from malformations up to fully developmental arrest. Possible interaction of polystyrene with biological membranes are considered the main cause of cyto- and genotoxicity, accompanied by potentially dramatic consequences for the reproductive fitness and success (Tallec et al., 2018). A recent review reports an accurate overview of more than 80 studies in which contamination by plastics and their debris appears to be one major contributors to the pollution of either marine and freshwaters. Their impact on organisms was shown to exert various effects on the growth, reproduction and development of aquatic animals, leading in long term to even species mortality (Chae & An, 2017). The rise of global temperature is an emerging phenomenon known as global warming. Together with the ocean acidification it is due to the increased release of carbon dioxide and other gases in the atmosphere and then in the seas due to the air-sea gas exchange. Reproductive processes are known to be temperature sensitive especially for male testicular function. In mouse, fertility potential declines at the air temperature increase and thermal waves were shown to affect birds (Hurley, McDiarmid, Friesen, Griffith, & Rowe, 2018) and insect sperm functionality as production, viability, and migration through the female genital tract. Surprisingly these thermal waves did not affect oocyte functions but the female sperm storage (Sales et al., 2018). Heat stress induces sperm defects especially in term of chromatin decondensation, which is an unstable conformation leading ultimately to fertility disorders especially related to epigenetic regulations. This has been highlighted in cattle (Rahman, Schellander, Luceño, & Van Soom, 2018) and human sperm where high levels of sperm chromatin and DNA damages have been associated with occupational exposure to heat sources (Rao et al., 2016). Several parameters of sperm quality appear to be affected by thermal stress also in marine mussels where the increase of few °C of the sea water induces gametogenesis and sperm physiology impairment (Boni, 2019; Boni, Gallo, Montanino, Macina, & Tosti, 2016; Múgica, Sokolova, Izagirre, & Marigómez, 2015). Female fertility seems to be less affected by heat stress with respect to male, however, evidence are presented in aquatic animals that global warming is able to modulate and highlight the endocrine disruptors affecting fitness, ovary maturation and ultimately reproduction success (Cardoso et al., 2017). Ocean acidification due to the excessive industrial production of CO2 in the atmosphere is causing a progressive decrease of seawater pH which is estimated to reach 7.8 at the end of this century (Foo, Byrne, Ricevuto, & Gambi, 2018; Gallo & Tosti, 2016). This represents a serious matter of concern due to the potential impact of global acidification on population decline and extinctions. Although numerous studies have evidenced an impact of reduced pH on calcification rates and shell structures of marine biota, still few studies have highlighted this effect on fertilization and embryo and larval development processes of mussels (Barros, Sobral, Range, Chícharo, & Matias, 2013; Gonzalez-Bernat, Lamare, & Barker, 2013). In particular, reduced pH appears to influence sperm motility, egg number, and size with consequent repercussion on the fertilization potential. Although the sensitivity of gametes to acidification is at present demonstrated in some studies, the adaptive potential of marine species (Foo & Byrne, 2016) and gamete resilience (Gallo et al., 2019, submitted) to this stressors is also an emerging topic accounting for the capacity of endangered species to continue to reproduce and persist in changing seas and oceans. Over the last decades, many authors have demonstrated the adverse effects of various different sources of pollution on reproduction and development in a broad range of taxa. Although new hints are available on the tolerance and adaptive capacity of species to environmental changes, most of the studies support the increasing impact of either chemical and physical pollution on the reproductive functions, the consequent decline of either male and female fertility, which in turn may drive biodiversity loss, and the threat to human health via different routes of transmission (Figure 1). Effects of environmental stressors on reproduction and development. A series of chemo-physical stressors as metals, nanoparticles, plastics, antifoulants, global warming, and ocean acidification impair gamete morphology and embryo/larval development [Color figure can be viewed at wileyonlinelibrary.com]