Maternal Transfer and Long-Term Population Effects of PCBs in Baltic Grey Seals Using a New Toxicokinetic–Toxicodynamic Population Model

Abstract

Empirical evidence has shown that historical exposure of polychlorinated biphenyls (PCBs) to Baltic grey seals not only severely affected individual fitness, but also population growth rates and most likely caused the retarded recovery rate of the depleted population for decades. We constructed a new model which we term a toxicokinetic–toxicodynamic (TKTD) population model to quantify these effects. The toxicokinetic sub-model describes in detail the bioaccumulation, elimination and vertical transfer from mother to offspring of PCBs and is linked to a toxicodynamic model for estimation of PCB-related damage, hazard and stress impacts on fertility and survival rates. Both sub-models were linked to a Leslie matrix population model to calculate changes in population growth rate and age structure, given different rates of PCB exposure. Toxicodynamic model parameters related to reproductive organ lesions were calibrated using published historical data on observed pregnancy rates in Baltic grey seal females. Compared to empirical data, the TKTD population model described well the age-specific bioaccumulation pattern of PCBs in Baltic grey seals, and thus, the toxicokinetic parameters, deduced from the literature, are believed to be reliable. The model also captured well the general effects of PCBs on historical population growth rates. The model showed that reduced fertility due to increased PCB exposure causes decreased vertical transfer from mother to offspring and in turn increased biomagnification in non-breeding females. The developed TKTD model can be used to perform population viability analyses of Baltic grey seals with multiple stressors, also including by-catches and different hunting regimes. The model can also be extended to other marine mammals and other contaminants by adjustments of model parameters and thus provides a test bed in silico for new substances.

120‐years of ecological monitoring data shows that the risk of overhunting is increased by environmental degradation for an isolated marine mammal population: The Baltic grey seal

“…Although the Atlantic grey seal populations have been extensively modelled, the Baltic grey seal has been largely omitted from such efforts since the early 2000s (Harding et al, 2007; Rossi et al, 2021; Thomas et al, 2019). Since then, the drivers of growth for the Baltic population have likely changed with large scale over‐fishing of key grey seal prey species, increased hunting, a reduced impact of pollution, and warmer winters as a result of climate change (Jüssi et al, 2008; Kauhala et al, 2017; Mauritsson et al, 2022; Olsen et al, 2018). The results of this study highlight the need to adopt dynamic and flexible management strategies to account for a changing environment, such as aiming to reduce hunting quotas over coming decades as good‐ice‐years become less frequent.…”

“…The age of first reproduction for female grey seals is generally around 5 years, with some variability, after which they are capable of giving birth to at most one pup per year (Bowen et al, 2006; Harwood & Prime, 1978). Annual birth‐rates for mature females in healthy populations are often reported above 90%, however, damage to reproductive organs by pollutants such as PCB can lead to rates as low as 9% (Bergman, 1999; Harwood & Prime, 1978; Kauhala et al, 2019; Mauritsson et al, 2022; Thomas et al, 2019). Birth‐rates vary between years and are lower for older seals (age 25+, Bowen et al, 2006).…”

“…In the past, pollution has resulted in fertility‐rates for mature female Baltic grey seals as low as 9%, rising to 60% in the 1990s (Bergman, 1999; Mauritsson et al, 2022). There is a continued threat to marine life in the Baltic of hazardous substance accumulation (Dietz et al, 2021; Sonne et al, 2020).…”

“…The history of the grey seal ( Halichoerus grypus ) is typical of a historically overexploited marine mammal (Boehme et al, 2012; den Heyer & Bowen, 2017; Harding et al, 2007; Mauritsson et al, 2022; Thomas et al, 2019). The species is divided into three main subpopulations: the Western Atlantic population along the coast of the United States and Canada, the Eastern Atlantic population centred around the British Isles, and the Baltic population in the Baltic Sea.…”

Advancing exposure assessment approaches to improve wildlife risk assessment

“…For reproductive females, energetic and nutritional demands can result in a necessary shift in diet to produce eggs or young which can enhance female exposure to contaminants as revealed for mercury, PCBs, and organochlorines in populations of American and Eurasian dippers (Morrissey et al, 2010). Both age and longevity will affect exposure in periods of potentially elevated levels of contaminants (Mauritsson et al, 2022), with chronic exposure and bioaccumulation resulting in elevated levels with age. The alteration of body condition of wildlife caused by migration, breeding, or aging renders necessary consideration of dynamic lipid or protein use and metabolism associated with life stage when addressing exposure to circulating toxicants.…”