In our systematic review, differences were observed among studies from different continents in their approach to studying EDCs in the environment. While some differences could be attributed to the total number of articles published by researchers from each continent, there were distinct disparities in sampling methods and focus on specific EDCs. Despite these differences, certain trends were consistent across all continents. For instance, water was the most-commonly sampled compartment, and the majority of studies examined the concentrations of pharmaceuticals in their samples.
Notably, continents differed in their frequencies of studying EDC samples from biota, although there was a common emphasis on fish as the primary animal group of interest in EDC research, likely due to being a global food source. It is worth mentioning that numerous laboratory studies were excluded from our systematic review due to their lack of environmental sampling or replication. Although laboratory studies can provide an initial insights into EDC dose responses in different animals, they may fail to replicate the level of exposure found in the wild, including the complex mixture of EDCs and the specific types of exposure (e.g. concentration and duration) encountered by wildlife (Miller et al., 2018). Additionally, it is important to note that EDCs are known to exhibit nonmonotonic dose responses, where greater effects can be observed at low doses that may not be apparent at higher doses (Vandenberg et al., 2012). While we recognise the importance of lab studies increasing our understanding of the potential impacts on wildlife to particular concentrations of EDCs, the complexities of environmental EDC exposure are difficult to replicate.
4.1 Differences in EDCs and sample types studied
Our systematic review shows that wildlife were sampled far less commonly than water in EDC research. Water was consistently the dominant sample type used across all continents, but different continents did not study EDCs in water at the same rates. Three-quarters of studies from Oceania sampled water, which was proportionally higher than other continents. The water matrix within an aquatic environment is considered to be the main source of EDC exposure to wildlife and humans (Gonsioroski et al., 2020), therefore it is not surprising that water is most-commonly sampled to monitor environmental EDC concentrations. Studies measuring EDCs in animals also varied in their proportion between continents. North America and Africa had the highest proportions of studies examining EDCs in animals (~ 33%). Sampling animals provides some clarity on how environmental EDC exposure may be impacting wildlife (Kloas, 2002; Marlatt et al., 2022; Tyler et al., 1998). As animals can metabolise some EDCs, concentrations found within animals may not necessarily reflect the concentration that the animal has been exposed to, and instead animals may experience physiological and behavioural changes that cannot be easily attributed to EDC causes.
Sediment and plants were sampled the least in EDC research. Given the ease in which sediment can be collected, sample rates were surprisingly low, but variable, across continents. Plants were sampled in only 11 studies across all continents, where the low sampling efforts may be due to their ability to accumulate EDCs but at different rates depending on the species. For example, the invasive curly leaf pond weed (Potamogeton illinoensis) has demonstrated greater accumulation of estrogenic compounds (averaging 66%) and bisphenol A (94%) than a native pondweed (Trueman & Erber, 2013).
4.2 Continental differences in EDCs studied
Since many pharmaceuticals are designed to be endocrine disruptors (i.e. oral contraceptives and hormone replacement therapy), they were, unsurprisingly, the most-frequently studied chemical group across all continents. After pharmaceuticals, the next most-commonly studied EDC differed among continents. In Asia, research on EDCs focused especially on bisphenol and alkylphenols. Bisphenol A (BPA) use for manufacturing plastics has grown substantially in Asia, particularly in China (Huang et al., 2012). Meanwhile, alkylphenols are still used widely in some parts of Asia for manufacturing, despite their ban in many countries (Bergé et al., 2012; Duan et al., 2014). The high use of BPA, and continued use of alkylphenols, likely explains why they are a commonly-studied EDCs in Asia. For North America, it is surprising how few studies examined BPA since the continent produces approximately 22.9% of the world’s total (Huang et al., 2012). For alkylphenols, it is similarly unusual that we found North America to have far fewer studies on the chemical group, as although regulations have aimed to decrease concentrations within the environment, the levels being recovered are still of environmental significance (Bergé et al., 2012). The next most commonly-studied chemical group in North America was organochlorine, followed closely by personal care products (PCPs). Organochlorine research has shown some of the best evidence for its endocrine disrupting potential on organisms, where exposure in the environment has been extensively studied in reptiles (particularly alligators) in North America (Guillette et al., 2000; Marlatt et al., 2022). Organochlorides were also the second most-commonly studied chemical group in Africa, and had a higher proportion of research undertaken compared to other continents. Organochlorines are often found in pesticides, and in African nations in particular, there is a lack of pesticide regulation and documented unsustainable farming practices that have led to concerns for community and environmental exposure (Williamson, Ball & Pretty 2008). The second most-commonly studied chemical groups for Oceania was PCPs, and for South America was BPA, however the reasoning for why they have been so heavily studied in these particular continents is unclear. It may be because there are far fewer studies coming from Oceania and South America, thus a lack of meaningful trends for these continents, with fewer than 100 studies looking at pharmaceuticals and < 50 studies for any other chemical group. Therefore, the proportion of chemical groups studied beyond pharmaceuticals may not necessarily be most important to those continents.
4.3 Differences in wildlife taxa studied
Environmental EDCs have profound impacts on exposed organisms when present at sufficient concentrations (Marlatt et al. 2022). Fish were the most-studied taxonomic group in EDC research across all continents. Aquatic biota, including fish, may be more vulnerable to EDC impacts due to continuous exposure in contaminated waterways, and fish have provided the strongest evidence that EDCs are impacting wild populations (Aris, Shamsuddin & Praveena 2014). Some of the earliest substantial evidence of wildlife impacts from EDC exposure was in the 1990s in flounder (Platichthys flesus) downstream of a sewage treatment facility in the United Kingdom (Allen et al. 1999). Male flounder were found to have significantly elevated vitellogenin concentrations and reproductive abnormalities when sampled from waterways exposed to sewage effluent (Allen et al. 1999). Fish are an important food source for many communities globally. Therefore, understanding how EDCs are impacting fish stocks, and the potential bioaccumulation of EDCs within fish, which may biomagnify in humans consuming fish, is crucial for both community health and food security (Aris et al. 2014; Lv et al. 2019). These studies demonstrate the importance of linking environmental surveillance of EDCs with lab-measured organism-level effects, rather than leaving environmental data to stand on their own as proxies of impacts.
Other aquatic organisms are likely to be similarly impacted by EDCs but studied far less often. Amphibians were one of the least-studied vertebrates for EDC concentrations, although existing research suggests they are just as vulnerable as fish to EDC exposure, and they are declining globally (Kloas 2002; Stuart et al. 2004). Amphibians are classic model organisms in endocrinology and developmental biology research, providing a solid foundation for mechanistic EDC research in other wild animals (Kloas 2002). Hayes et al., (2002) demonstrated the feminization of Leopard frogs (Rana pipiens) associated with waterborne Atrazine (a common herbicide) in parts of the USA. Their study also found a higher rate of male Leopard frogs having reproductive abnormalities in areas where Atrazine sales were greater than 0.4 kg/km− 2 and present at 0.2 p.p.b within waterbodies (Hayes et al., 2002). Other studies have provided further supportive evidence that EDCs impact frog populations. For example, the proportion of intersex cricket frogs (Acris crepitans) in the USA increased during the industrial growth era with the extensive use of EDCs like PCBs, DDT, and organochlorine pesticides (Reeder et al. 2005). Even in suburban environments, where sources of EDCs are less clear, sensitive frog populations still became feminized from the exposure (Lambert et al., 2015).
Reptiles were understudied globally, with almost 80% of reptile EDC studies come from North America. In North America, the physiological impacts of EDCs on aquatic reptiles like Chelonians and Crocodilians have been documented (Guillette, 2006; Irwin et al., 2001). Many reptile species have high site fidelity, carnivorous diets, and long life spans that presumably heighten their EDC exposure, and consequently, are excellent sentinel species for examining long-term EDC exposure (Hopkins, 2000). The most extensively studied reptile have been in alligators in Lake Apopka (Florida, USA), a pesticide-contaminated lake, where their exposure to EDCs has led to altered plasma hormone concentrations and developmental defects that are shown in hatchlings (Guillette et al., 2000).
To date, literature on EDC bioaccumulation and biomagnification in animals is scarce. From the limited literature available, bioaccumulation of EDCs has been documented in fish (Wang & Gardinali, 2013), crustaceans (Vernouillet et al., 2010), algae (Vernouillet et al., 2010), turtles (Beale et al., 2022) and molluscs (de Solla et al., 2016). Understandably, from a human-centered perspective, there is greater importance in understanding bioaccumulation in seafood to ensure human populations are not consuming potentially high doses of EDCs (Ebele et al., 2017). Physiological differences across species will likely underlie variation in how contaminants bioaccumulate and biomagnify (Lv et al., 2019; Puckowski et al., 2016). For example, invertebrates are presumed to have greater rates of EDC bioaccumulation than vertebrates since they have a greater surface-to-volume ratio (Cuvillier-hot & Lenoir, 2020). Invertebrates are generally easier to study than vertebrates, since they are smaller, more abundant, and usually have fewer regulatory permit requirements. However, there are limitations to our understanding of EDC impacts on invertebrates, due to our current inadequate understanding of their endocrinology, which is fundamental for EDC research (Ford & Leblanc, 2020a; Hutchinson, 2007). For abiotic compartments to be an effective proxy to understand when concentrations of EDCs are excessive or likely to cause biological harm, more research is needed investigating the impacts of environmental EDC exposure across a range of wildlife.
4.4 Conclusion
Our systematic review highlights the extent of environmental EDC research to date, where less than a third of studies have examined EDC exposure and impacts on wildlife. Some of the earliest studies on the impacts of EDC exposure on wildlife occurred in the 1970s (Blaber, 1970; Marlatt et al., 2022). Since then, studies have prioritised monitoring water to determine EDC concentrations within the environment as a proxy for wildlife exposure, and far fewer studies have directly measured EDC accumulation or impacts on wildlife. Some of the limited progress on EDC exposure and its impacts on wildlife may be explained by the knowledge gaps on foundational endocrinology for some organisms (Ford & Leblanc, 2020b), and the lack of standardisation of analytical methods in ecotoxicology (Miller et al., 2018).
A critical area for future research is to develop baselines for converting abiotic EDC concentrations into dose-response curves for key organisms of local interest, which could then act as indicator or sentinel species for a given environment. Such baselines would provide two clear improvements over current sampling, which appears to be relatively unstrategic, at least on a global scale. First, having a baseline to refer to would greatly improve the relevancy of abiotic-only proxy sampling, especially in regions or systems where examining EDC impacts on wildlife more directly is prohibitively expensive. Second, baselines would allow calibration of the EDC concentrations used in laboratory studies aiming to investigate real-world impacts of EDC exposure in wildlife, to prevent both over- and under-estimation of potential EDC impacts.