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.

The Baltic Sea is home to a genetically isolated and morphologically distinct grey seal population. This population has been the subject of 120-years of careful documentation, from detailed records of bounty statistics to annual monitoring of health and abundance. It has also been exposed to a range of well-documented stressors, including hunting, pollution and climate change. To investigate the vulnerability of marine mammal populations to multiple stressors, data series relating to the Baltic grey seal population size, hunt and health were compiled, vital demographic rates were estimated, and a detailed population model was constructed. The Baltic grey seal population fell from approximately 90,000 to as few as 3000 individuals during the 1900s as the result of hunting and pollution. Subsequently, the population has recovered to approximately 55,000 individuals. Fertility levels for mature females have increased from 9% in the 1970s to 86% at present. The recovery of the population has led to demands for increased hunting, resulting in a sudden increase in annual quotas from a few hundred to 3550 in 2020. Simultaneously, environmental changes, such as warmer winters and reduced prey availability due to overfishing, are likely impacting fecundity and health. Future population development is projected for a range of hunting and environmental stress scenarios, illustrating how hunting, in combination with environmental degradation, can lead to population collapse. The current combined hunting quotas of all Baltic Nations caused a 10% population decline within three generations in 100% of simulations. To enable continued recovery of the population, combined annual quotas of less than 1900 are needed, although this quota should be re-evaluated annually as monitoring of population size and seal health continues. Sustainable management of long-lived slowly growing species requires an understanding of the drivers of population growth and the repercussions of management decisions over many decades. The case of the Baltic grey seal illustrates how long-term ecological time series are pivotal in establishing historical baselines in population abundance and demography to inform sustainable management.

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

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.

A Unifying Framework for Estimating Generation Time in Age-Structured Populations: Implications for Phylogenetics and Conservation Biology.

AbstractGeneration time is a measure of the pace of life and is used to describe processes in population dynamics and evolution. We show that three commonly used mathematical definitions of generation time in age-structured populations can produce different estimates of up to several years for the same set of life history data. We present and prove a mathematical theorem that reveals a general order relation among the definitions. Furthermore, the exact population growth rate at the time of sampling influences estimates of generation time, which calls for attention. For phylogenetic estimates of divergence times between species, included demographic data should be collected when the population growth rate for each species is most common and typical. In conservation biology, demographic data should be collected during phases of population decline in declining species, contrary to common recommendations to use predisturbance data. The results can be used to improve the International Union for Conservation of Nature's recommendation in parameterizing models for evaluating threat categories of threatened species and to avoid underestimating extinction risk.

Life cycle bioenergetics of the gray seal (Halichoerus grypus) in the Baltic Sea: Population response to environmental stress.

Wildlife population dynamics are shaped by multiple natural and anthropogenic factors, including predation, competition, stressful life history events, and external environmental stressors such as diseases and pollution. Marine mammals such as gray seals rely on extensive blubber layers for insulation and energy storage, making this tissue critical for survival and reproduction. This lipid rich blubber layer also accumulates hazardous fat soluble pollutants, such as polychlorinated biphenyls (PCBs), that can directly impact adipose function or be mobilized during periods of negative energy balance or transferred to offspring to exert further impacts on target tissues or vulnerable life stages. To predict how marine mammals will respond to ecological and anthropogenic stressors, it is necessary to use process-based modelling approaches that integrate environmental inputs, full species life history, and stressor impacts with individual dynamics of energy intake, storage, and utilization. The purpose of this study was to develop a full lifecycle dynamic energy budget and individual based model (DEB-IBM) that captured Baltic gray seal physiology and life history, and showcase potential applications of the model to predict population responses to select stressors known to threaten gray seals and other marine mammals around the world. We explore variations of three ecologically important stressors using phenomenological simulations: food limitation, endocrine disrupting chemicals that reduce fertility, and infectious disease. Using our calibrated DEB-IBM for Baltic gray seals, we found that continuous incremental food limitation can be more detrimental to population size than short random events of starvation, and further, that the effect of endocrine disruptors on population growth and structure is delayed due to bioaccumulation, and that communicable diseases significantly decrease population growth even when spillover events are relatively less frequent. One important finding is the delayed effect on population growth rate from some stressors, several years after the exposure period, resulting from a decline in somatic growth, increased age at maturation and decreased fecundity. Such delayed responses are ignored in current models of population viability and can be important in the correct assessment of population extinction risks. The model presented here provides a test bed on which effects of new hazardous substances and different scenarios of future environmental change affecting food availability and/or seal energetic demands can be investigated. Thus, the framework provides a tool for better understanding how diverse environmental stressors affect marine mammal populations and can be used to guide scientifically based management.

Multiple stressors and data deficient populations; a comparative life-history approach sheds new light on the extinction risk of the highly vulnerable Baltic harbour porpoises (Phocoena phocoena).

Many endangered marine mammal populations are difficult to study, spread out over large areas, and capturing them for branding and research purposes would be unethical. Yet, they are in urgent need for assessment and conservation actions. We suggest collecting data from other more abundant populations of the same species, with careful consideration of body size, age at sexual maturity, and ecological conditions to produce scientifically sound best approximations of vital rates of data deficient endangered populations. The genetically distinct Baltic Sea harbour porpoise population amounts to about 500 animals and is classified as 'Critically Endangered' according to the IUCN red list. Data deficiency on nearly all demographic parameters have precluded systematic investigations of the relative importance of stressors affecting population viability. We took a comparative life history approach and investigated the phenotypic plasticity in somatic and demographic vital rates of seven larger, well studied North Atlantic harbour porpoise populations, enabling us to approximate the missing pieces of the life history of the Baltic population. We parameterized a stochastic, individual-based population model, and performed a population viability analysis for a range of biologically realistic parameter values and scenarios of environmental stressors. The baseline scenario was based on the most representative samples of healthy harbour porpoise populations and challenged with three different levels of bycatches. Due to high levels of endocrine disruptive contaminants observed in Baltic harbour porpoises, we also investigated the effect of a possible reduction in fecundity. Subsequently, the combined effects of bycatches and reduced fecundity were investigated in terms of population growth rate and quasi-extinction risk. The Baltic harbour porpoise population is viable in the baseline scenario without anthropogenic stressors. However, even the lowest estimated bycatch level of 7 individuals per year will lead to a population collapse to ≤50 animals with high probability (0.4-1.0) over the next century, assuming an intermediate or low (<73%) fecundity. Adult survival is of critical importance and mitigation of fishery impacts and reduction of anthropogenic disturbances in the identified main breeding areas are recommended.

Health effects from contaminant exposure in Baltic Sea birds and marine mammals: A review.

Here we review contaminant exposure and related health effects in six selected Baltic key species. Sentinel species included are common eider, white-tailed eagle, harbour porpoise, harbour seal, ringed seal and grey seal. The review represents the first attempt of summarizing available information and baseline data for these biomonitoring key species exposed to industrial hazardous substances focusing on anthropogenic persistent organic pollutants (POPs). There was only limited information available for white-tailed eagles and common eider while extensive information exist on POP exposure and health effects in the four marine mammal species. Here we report organ-tissue endpoints (pathologies) and multiple biomarkers used to evaluate health and exposure of key species to POPs, respectively, over the past several decades during which episodes of significant population declines have been reported. Our review shows that POP exposure affects the reproductive system and survival through immune suppression and endocrine disruption, which have led to population-level effects on seals and white-tailed eagles in the Baltic. It is notable that many legacy contaminants, which have been banned for decades, still appear to affect Baltic wildlife. With respect to common eiders, changes in food composition, quality and contaminant exposure seem to have population effects which need to be investigated further, especially during the incubation period where the birds fast. Since new industrial contaminants continuously leak into the environment, we recommend continued monitoring of them in sentinel species in the Baltic, identifying possible effects linked to climate change, and modelling of population level effects of contaminants and climate change.

Genomics of host-pathogen interactions: challenges and opportunities across ecological and spatiotemporal scales.

Evolutionary genomics has recently entered a new era in the study of host-pathogen interactions. A variety of novel genomic techniques has transformed the identification, detection and classification of both hosts and pathogens, allowing a greater resolution that helps decipher their underlying dynamics and provides novel insights into their environmental context. Nevertheless, many challenges to a general understanding of host-pathogen interactions remain, in particular in the synthesis and integration of concepts and findings across a variety of systems and different spatiotemporal and ecological scales. In this perspective we aim to highlight some of the commonalities and complexities across diverse studies of host-pathogen interactions, with a focus on ecological, spatiotemporal variation, and the choice of genomic methods used. We performed a quantitative review of recent literature to investigate links, patterns and potential tradeoffs between the complexity of genomic, ecological and spatiotemporal scales undertaken in individual host-pathogen studies. We found that the majority of studies used whole genome resolution to address their research objectives across a broad range of ecological scales, especially when focusing on the pathogen side of the interaction. Nevertheless, genomic studies conducted in a complex spatiotemporal context are currently rare in the literature. Because processes of host-pathogen interactions can be understood at multiple scales, from molecular-, cellular-, and physiological-scales to the levels of populations and ecosystems, we conclude that a major obstacle for synthesis across diverse host-pathogen systems is that data are collected on widely diverging scales with different degrees of resolution. This disparity not only hampers effective infrastructural organization of the data but also data granularity and accessibility. Comprehensive metadata deposited in association with genomic data in easily accessible databases will allow greater inference across systems in the future, especially when combined with open data standards and practices. The standardization and comparability of such data will facilitate early detection of emerging infectious diseases as well as studies of the impact of anthropogenic stressors, such as climate change, on disease dynamics in humans and wildlife.

Phylogenomic insights to the origin and spread of phocine distemper virus in European harbour seals in 1988 and 2002.

The 1988 and 2002 phocine distemper virus (PDV) outbreaks in European harbour seals Phoca vitulina are among the largest mass mortality events recorded in marine mammals. Despite its large impact on harbour seal population numbers, and 3 decades of studies, many questions regarding the spread and temporal origin of PDV remain unanswered. Here, we sequenced and analysed 7123 bp of the PDV genome, including the coding and non-coding regions of the entire P, M, F and H genes in tissues from 44 harbour seals to shed new light on the origin and spread of PDV in 1988 and 2002. The phylogenetic analyses trace the origin of the PDV strain causing the 1988 outbreak to between May 1987 and April 1988, while the origin of the strain causing the 2002 outbreak can be traced back to between June 2001 and May 2002. The analyses further point to several independent introductions of PDV in 1988, possibly linked to a southward mass immigration of harp seals in the winter and spring of 1987-1988. The vector for the 2002 outbreak is unknown, but the epidemiological analyses suggest the subsequent spread of PDV from the epicentre in the Kattegat, Denmark, to haul-out sites in the North Sea through several independent introductions.

Bio accumulation of radioactive caesium in marine mammals in the Baltic Sea - Reconstruction of a historical time series.

Radionuclides from the Chernobyl accident in 1986 still circulate in the Baltic marine ecosystem and activity levels in water, sediments and fish species such as herring and perch are monitored annually. However, the activity levels of radionuclides in marine mammals have only been sporadically reported. Tissue samples from a museum collection were analysed in two species of seals, and the trends over time in activity level of radioactive caesium (Cs-137) after the Chernobyl accident were reconstructed. We also performed a literature review summarizing activity levels in marine mammals world-wide. We found activity concentrations of Cs-137 in Baltic ringed seals and grey seals to be elevated also in the most recent samples, and during the entire study period measurements ranged between 19 and 248 Bq/kg wet weight. A declining trend in time over the last 30 years follow the general trend of decline in activity levels in other Baltic biota. Accumulation was found to be species specific in the two seal species studied, with 9 times higher activity concentration in grey seals compared to herring, and 3.5 times higher in ringed seals compared to herring. We discuss potential paths and rates of bioaccumulation of radioactive caesium in the Baltic Sea including species specific prey choice of the two seal species and estimate life time exposure. The study contributes one important piece of information to predictive models in risk assessments for nuclear accidents.

Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity.

The length of intervals between epidemic outbreaks of infectious diseases is critical in epidemiology. In several species of marine mammals and birds, it is pivotal to also consider the life history of the species of concern, as the contact rate between individuals can have a seasonal flux, for example, due to aggregations during the breeding season. Recently, particular interest has been given to the role of the dynamics of immunity in determining the intervals between epidemics in wild animal populations. One potentially powerful, but often neglected, process in this context is the maternal transfer of immunity. Here, we explore theoretically how the transfer of maternal antibodies can delay the recurrence of epidemics using Phocine Distemper in harbor seals as an example of a system in which epidemic outbreaks are followed by pathogen extinction. We show that the presence of temporarily protected newborns can significantly increase the predicted interval between epidemics, and this effect is strongly dependent on the degree of synchrony in the breeding season. Furthermore, we found that stochasticity in the onset of epidemics in combination with maternally acquired immunity increases the predicted intervals between epidemics even more. These effects arise because newborns with maternal antibodies temporarily boost population level immunity above the threshold of herd immunity, particularly when breeding is synchronous. Overall, our results show that maternal antibodies can have a profound influence on the dynamics of wildlife epidemics, notably in gregarious species such as many marine mammals and seabirds.

Capital and income breeding: the role of food supply.

An aspect of life history that has seen increasing attention in recent years is that of strategies for financing the costs of offspring production. These strategies are often described by a continuum ranging from capital breeding, in which costs are met purely from endogenous reserves, to income breeding, in which costs are met purely from concurrent intake. A variety of factors that might drive strategies toward a given point on the capital-income continuum has been reviewed, and assessed using analytical models. However, aspects of food supply, including seasonality and unpredictability, have often been cited as important drivers of capital and income breeding, but are difficult to assess using analytical models. Consequently, we used dynamic programming to assess the role of the food supply in shaping offspring provisioning strategies. Our model is parameterized for a pinniped (one taxon remarkable for the range of offspring-provisioning strategies that it illustrates). We show that increased food availability, increased seasonality, and, to a lesser extent, increased unpredictability can all favor the emergence of capital breeding. In terms of the conversion of energy into offspring growth, the shorter periods of care associated with capital breeding are considerably more energetically efficient than income breeding, because shorter periods of care are associated with a higher ratio of energy put into offspring growth to energy spent on parent and offspring maintenance metabolism. Moreover, no clear costs are currently associated with capital accumulation in pinnipeds. This contrasts with general assumptions about endotherms, which suggest that income breeding will usually be preferred. Our model emphasizes the role of seasonally high abundances of food in enabling mothers to pursue an energetically efficient capital-breeding strategy. We discuss the importance of offspring development for dictating strategies for financing offspring production.

Collapse of a marine mammal species driven by human impacts.

Understanding historical roles of species in ecosystems can be crucial for assessing long term human impacts on environments, providing context for management or restoration objectives, and making conservation evaluations of species status. In most cases limited historical abundance data impedes quantitative investigations, but harvested species may have long-term data accessible from hunting records. Here we make use of annual hunting records for Caspian seals (Pusa caspica) dating back to the mid-19(th) century, and current census data from aerial surveys, to reconstruct historical abundance using a hind-casting model. We estimate the minimum numbers of seals in 1867 to have been 1-1.6 million, but the population declined by at least 90% to around 100,000 individuals by 2005, primarily due to unsustainable hunting throughout the 20(th) century. This collapse is part of a broader picture of catastrophic ecological change in the Caspian over the 20(th) Century. Our results combined with fisheries data show that the current biomass of top predators in the Caspian is much reduced compared to historical conditions. The potential for the Caspian and other similar perturbed ecosystems to sustain natural resources of much greater biological and economic value than at present depends on the extent to which a number of anthropogenic impacts can be harnessed.

Linking climate trends to population dynamics in the Baltic ringed seal: impacts of historical and future winter temperatures.

A global trend of a warming climate may seriously affect species dependent on sea ice. We investigated the impact of climate on the Baltic ringed seals (Phoca hispida botnica), using historical and future climatological time series. Availability of suitable breeding ice is known to affect pup survival. We used detailed information on how winter temperatures affect the extent of breeding ice and a climatological model (RCA3) to project the expected effects on the Baltic ringed seal population. The population comprises of three sub-populations, and our simulations suggest that all of them will experience severely hampered growth rates during the coming 90 years. The projected 30, 730 seals at the end of the twenty-first century constitutes only 16 % of the historical population size, and thus reduced ice cover alone will severely limit their growth rate. This adds burden to a species already haunted by other anthropogenic impacts.

Detecting density dependence in recovering seal populations.

Time series of abundance estimates are commonly used for analyses of population trends and possible shifts in growth rate. We investigate if trends in age composition can be used as an alternative to abundance estimates for detection of decelerated population growth. Both methods were tested under two forms of density dependence and different levels of environmental variation in simulated time series of growth in Baltic gray seals. Under logistic growth, decelerating growth could be statistically confirmed after 16 years based on population counts and 14 years based on age composition. When density dependence sets in first at larger population sizes, the age composition method performed dramatically better than population counts, and a decline could be detected after 4 years (versus 10 years). Consequently, age composition analysis provides a complementary method to detect density dependence, particularly in populations where density dependence sets in late.

Seasonal activity budget of adult baltic ringed seals.

Although ringed seals are important components in oceanic and fresh water ecosystems at high latitudes, little is known about how they exploit these harsh environments. Seasonal activity and diving behaviour of 19 adult Baltic ringed seals were studied by satellite telemetry. We elaborated an activity budget for ten months of the year, extending over the period from moult to the breeding season. Seals from three main regions showed explicit site fidelity and the distributions of animals tagged from different areas did not overlap, suggesting separate stocks. Both the mean duration and the mean depth of dives peaked in June and July. Seals spent 70% (females) to 85% (males) of their time diving in June and July which decreased to 50% in late autumn. Less than one percent of dives exceeded 10 min in females, while 10% of male dives lasted longer than 10 min in June to September. Less than one percent of dives lasted for more than 25 min. Both females and males were most active during day time and hauled out predominantly during the night. Activity patterns during the summer are suggested to be correlated to energy accumulation and prey availability. The information on seasonal activity budget is crucial for developing population energetic models where interactions between ringed seals and other trophic levels can be evaluated.

The scaling of diving time budgets: insights from an optimality approach.

Simple scaling arguments suggest that, among air-breathing divers, dive duration should scale approximately with mass to the one-third power. Recent phylogenetic analyses appear to confirm this. The same analyses showed that duration of time spent at the surface between dives has scaling very similar to that of dive duration, with the result that the ratio of dive duration to surface pause duration is approximately mass invariant. This finding runs counter to other arguments found in the diving literature that suggest that surface pause duration should scale more positively with mass, leading to a negative scaling of the dive-pause ratio. We use a published model of optimal time allocation in the dive cycle to show that optimal decisions can predict approximate mass invariance in the dive-pause ratio, especially if metabolism scales approximately with mass to the two-thirds power (as indicated by some recent analyses) and oxygen uptake is assumed to have evolved to supply the body tissues at the required rate. However, emergent scaling rules are sensitive to input parameters, especially to the relationship between the scaling of metabolism and oxygen uptake rate at the surface. Our results illustrate the utility of an optimality approach for developing predictions and identifying key areas for empirical research on the allometry of diving behavior.

Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance.

Disease can generate intense selection pressure on host populations, but here we show that acquired immunity in a population subject to repeated disease outbreaks can impede the evolution of genetic disease resistance by maintaining susceptible genotypes in the population. Interference between the life-history schedule of a species and periodicity of the disease has unintuitive effects on selection intensity, and stochasticity in outbreak period further reduces the rate of spread of disease-resistance alleles. A general age-structured population genetic model was developed and parameterized using empirical data for phocine distemper virus (PDV) epizootics in harbor seals. Scenarios with acquired immunity had lower levels of epizootic mortality compared with scenarios without acquired immunity for the first PDV outbreaks, but this pattern was reversed after about five disease cycles. Without acquired immunity, evolution of disease resistance was more rapid, and long-term population size variation is efficiently dampened. Acquired immunity has the potential to significantly influence rapid evolutionary dynamics of a host population in response to age-structured disease selection and to alter predicted selection intensities compared with epidemiological models that do not consider such feedback. This may have important implications for evolutionary population dynamics in a range of human, agricultural, and wildlife disease settings.

A unifying framework for metapopulation dynamics.

Many biologically important processes, such as genetic differentiation, the spread of disease, and population stability, are affected by the (natural or enforced) subdivision of populations into networks of smaller, partly isolated, subunits. Such "metapopulations" can have extremely complex dynamics. We present a new general model that uses only two functions to capture, at the metapopulation scale, the main behavior of metapopulations. We show how complex, structured metapopulation models can be translated into our generalized framework. The metapopulation dynamics arising from some important biological processes are illustrated: the rescue effect, the Allee effect, and what we term the "antirescue effect." The antirescue effect captures instances where high migration rates are deleterious to population persistence, a phenomenon that has been largely ignored in metapopulation conservation theory. Management regimes that ignore a significant antirescue effect will be inadequate and may actually increase extinction risk. Further, consequences of territoriality and conspecific attraction on metapopulation-level dynamics are investigated. The new, simplified framework can incorporate knowledge from epidemiology, genetics, and population biology in a phenomenological way. It opens up new possibilities to identify and analyze the factors that are important for the evolution and persistence of the many spatially subdivided species.