One area of science that often fails to reach public emotional interest is ecotoxicology. The bioaccumulation of toxic trace elements and persistent organic pollutants (POPs) is an invisible killer that is slowly changing our earth’s ecosystems, particularly those in marine environments

Unlike the infamous plastic pandemic, or the climate change crisis, many are unaware of the threats of toxic chemicals to biological systems, and how these are impacting the health of vital players in marine food webs. While some organic pollutants, such as organochlorine pesticides, have been widely banned since the 1990s, international legislation controlling usage was not implemented until the Stockholm Convention came into effect in 2004 (USEPA, 2009). Every year, new chemical structures are synthesised in such quantities that legislation cannot keep up. The continued increase in chemical manufacture globally has resulted in unprecedented levels of chemical pollutants in waterways and oceans, often resulting in bioaccumulation in the tissues of apex predators.

Since implementation of the Stockholm Convention on POPs, concern about organic and inorganic pollutants has sparked multiple studies into the sequestration of toxins in animal tissues. Recent research is finding that chemical pollutants may have long term effects on population health and survival. Bull Shark (Carcharhinus leucas) and Tiger Shark (Galeocerdo cuvier) embryos were analysed in a 2018-19 study alongside maternal tissues (Chynel et al., 2020). This research, completed by Chynel and associates, was able to determine that pregnant adult sharks underwent maternal offloading through sharing of nutrients with developing embryos, causing prenatal contamination of toxic compounds in their pups.

“This research was able to determine that pregnant adult sharks underwent maternal offloading causing prenatal contamination of toxic compounds in their pups”

What does this mean?

No, really – what the hell are POPs and EOCs?
Persistent organic pollutants are defined by their toxicity, stability in the environment, and ability to travel long distances and accumulate in organisms. POPs are often observed contaminating habitats a long way from the source of emission, and are often termed ‘worldwide contaminants’ for this reason. As most known POPs (identified by the Stockholm convention) are banned in the majority of developed countries, new chemicals are being synthesised to take their place. The threat of these Emerging Organic Chemicals (EOCs) in terms of their ability to interact with biological systems, is unknown.

Sharks are high trophic level predators, therefore the sequestration of POPs and EOCs in shark prey results in biomagnification of these compounds between sharks and their prey. In toxic concentrations, these chemicals can cause reproductive impairment or failure (stillbirths and birth defects), altered gene expression and growth inhibition due to their interaction with the endocrine system (Tsai, 2010).

What does this mean for neonates and future shark generations?
In this study, published in 2021 in ‘Science of the total Environment,’ (Vol. 751), both legacy POPs and EOCs were measured in two sympatric shark species (Chynel et al., 2020). Significant maternal offloading was observed in the Bull Shark. This route of decontamination for the mother results in early exposure to pups and consequently potential development issues (Chynel et al., 2020).

“Maternal offloading contributes to the global organic contaminant cycle via chemical transfer to offspring prior to other external exposure,” (Chynel et al., 2020).”

How it Works

Bull Sharks and Tiger Sharks exhibit different embryonic nourishment strategies. Bull sharks are viviparous yolk-sac placental, and nourish their young through transmembrane transfer from the placenta after yolk stores are depleted. Tiger sharks are the only requiem sharks that do not have a placenta. They are ovoviviparous aplacental with lecithotrophic nutritional modes (Chynel et al., 2020). This means that multiple eggs are fertilised and each is nourished in the womb by a separate yolk sac rather than a placenta, but the mother will still give birth to live young. Previous studies in marine mammals show that placental nourishment may result in a 30-80% contaminant offload rate (Lyons & Lowe, 2013). While aplacental shark species do not undergo continuous exchange with their embryos through blood, they mobilise lipids to nourish the yolk sack prior to fertilisation (Naidoo et al., 2017). Most organic contaminants are lipophilic and consequently associate with lipids. In sharks, there is a large concentration of lipids in the liver as it serves to control buoyancy in the absence of a swim bladder or lungs. During reproduction, a large quantity of these lipids are mobilised to provide energy and nourishment to the yolk sac and embryos resulting in embryonic contamination. 

The Chynel et al., study revealed that female Bull Sharks were able to decontaminate during gestation, indicating significant maternal offload to pups (Chynel et al., 2020). However, Tiger shark embryos displayed lipophilic contaminant concentrations two times higher than bull shark embryos, indicating that yolk-sac nourishment may allow for lipid mobilised contamination of embryos during maternal offloading in the absence of placental connection (Chynel et al., 2020).

“Concentrations of all chlorinated compounds and PFCAs […] were 2 to 7 times higher […] in tiger shark embryos than in the mother”

What Threat Does this Pose?

Sharks are keystone species and drivers of ecosystem health. If fecundity decreases along with reproductive success, this will have a huge impact on a taxa that is already under extreme anthropogenic pressure. Population decreases could throw the entire marine ecosystem out of balance, increasing the abundance of grazers and decreasing biodiversity. From a human health perspective, these findings are also a concern. Globally, the large shark fishery market (which itself is problematic for shark population survival) supplies shark flesh for traditional cuisine. The concentration of toxins, including POPs, in shark tissues are often above food standard regulations (Kim et al., 2019), and eating them poses a threat to human health.

What Now?

Research into the sequestration and long-term effects of contaminants, as well as understanding the potential threats of emerging compounds, is crucial. In order to prevent the collapse of food webs more resources must be allocated to understanding the impact of these pollutants and what we can do to mitigate their effects on marine ecosystems.

References

Chynel, M., Munschy, C., Bely, N., Héas-Moisan, K., Pollono, C., & Jaquemet, S. (2021). Legacy and emerging organic contaminants in two sympatric shark species from Reunion Island (Southwest Indian Ocean): Levels, profiles and maternal transfer. Science of The Total Environment, 751, 141807. doi:https://doi.org/10.1016/j.scitotenv.2020.141807

Kim, S. W., Han, S. J., Kim, Y., Jun, J. W., Giri, S. S., Chi, C., Yun, S., Kim, H. J., Kim,

S. G., Kang, J. W., Kwon, J., Oh, W. T., Cha, J., Han, S., Lee, B. C., Park, T., Kim, B. Y., & Park, S. C. (2019). Heavy metal accumulation in and food safety of shark meat from Jeju island, Republic of Korea. PloS one, 14(3), e0212410. https://doi.org/10.1371/journal.pone.0212410

 Lyons, K., & Lowe, C. G. (2013). Mechanisms of maternal transfer of organochlorine contaminants and mercury in the common thresher shark (Alopias vulpinus). Canadian journal of fisheries and aquatic sciences, 70(12), 1667-1672.

Naidoo, K., Chuturgoon, A., Cliff, G., Singh, S., Ellis, M., Otway, N., . . . Gregory, M. (2017). Possible maternal offloading of metals in the plasma, uterine and capsule fluid of pregnant ragged-tooth sharks (Carcharias taurus) on the east coast of South Africa. Environmental Science and Pollution Research, 24(20), 16798-16805. doi:10.1007/s11356-017-9281-1

Tsai, W.-T. (2010). Current Status and Regulatory Aspects of Pesticides Considered to be Persistent Organic

Pollutants (POPs) in Taiwan. International Journal of Environmental Research and Public Health, 7(10), 3615–3627. MDPI AG. Retrieved from http://dx.doi.org/10.3390/ijerph7103615

United States Environmental Protection agency. (2009). Persistent Organic Pollutants: A Global Issue, A Global Response. Retrieved from https://www.epa.gov/international-cooperation/persistent-organic-pollutants-global-issue-global-response