By Sophie Watson
As one of the most ice-dependent Arctic marine mammals, polar bears (Ursus maritimus) are an iconic species of climate change. The media is peppered with evidence of the damaging effects of climate change on this sentinel species, often citing habitat loss, shifts in prey availability/abundance, and transitions in inter-species interactions. We know that polar bears require sea ice for long-distance movements and accessing their typical prey items of ringed seal (Pusa hispida), bearded seal (Erignathus barbatus) and occasionally beluga whale (Delphinapterus leucas). We also know that for polar bears belonging to the southern Beaufort Sea subpopulation, substantial declines in the spatial and temporal availability of sea ice in summer and fall (extending well beyond the biologically productive continental shelf) have driven a divide in polar bear behaviour. Some bears continue to select the retreating ice habitat to hunt (‘offshore bears’) while others instead adopt a novel behaviour for this subpopulation and move to coastal onshore habitat during the reduced ice period (‘onshore bears’). For some researchers, this alarming divide in behaviour prompted the notion that to we need to act fast and think big. For a few of us however, it impelled us to think small. Microscopic, in fact.
The gut microbiota, the community of microscopic bacteria inhabiting the gut, has a long co-evolutionary association with its host, and plays a critical role in individual health. For example, most complex carbohydrates and plant polysaccharides can only be broken down by the gut microbiota. In laboratory mice, a dearth of gut bacteria correlates with abnormal immune cell counts and abnormal spleen node size. Furthermore, microbes within the gastrointestinal tract play an important role by filling available microbiological niches, therefore limiting competition against the colonisation of potentially harmful microorganisms. In effect, the regular intestinal development and function of an individual is attributed to the gut microbiota, the composition and diversity of which are a function of complex interactions between host and environment. Changes in a host’s environment can therefore lead to shifts in the gut microbiota which can have substantial effects on host health. For onshore polar bears, one of the most prominent changes to their environment is the shift in food resources available to them.
We know that onshore bears are associated with a range of dietary items that offshore bears are unable to access, notably ‘bone piles’, the remains of locally-harvested bowhead whales (Balaena mysticetus), along with the carcasses of fish, birds and caribou (Rangifer tarandus). Shifts in diet have the potential to alter polar bear gut microbiota, potentially making the microbiota less specialist in its evolved role. Dietary changes can also alter the contaminants and parasites that polar bears acquire. For example, ringed seals (available only to offshore bears) occupy a high trophic position and so typically bioaccumulate higher levels of contaminants than species lower in the trophic chain such as the filter feeders (i.e. bowhead whales) and herbivores (i.e. caribou), which are available only to onshore bears. In addition, bone piles, foraged on by onshore bears, are utilised as a food resource by other terrestrial species and lie within comparatively close range of human settlements. As such, onshore bears are potentially exposed to (and therefore at greater risk of infection from) novel parasites carried by terrestrial species, including humans and their domestic pets. For example, our USGS collaborator, Todd Atwood, and his colleagues found that onshore bears have a greater risk of exposure to Toxoplasma gondii, a parasite usually found in domestic cats that can accidentally ‘spillover’ into other species, including humans, where symptoms can include vision loss, birth defects and behavioural changes. We know from other species that parasitic infections dramatically alter the gut microbiota while contaminants can inhibit the growth of a variety of beneficial gut bacteria, and even cause the gut microbiota to become unbalanced, leading to poor health.
Despite our understanding of the health importance of these microbes, little is understood of the polar bear gut microbiota. Our research revealed that for southern Beaufort Sea polar bears, bacterial diversity (i.e. the number of different bacterial species present) and composition are significantly different in the gut of onshore bears compared to offshore bears – i.e. those that exhibit the ‘normal’ behaviour of remaining on the sea ice year-round. Specifically, we see a significant increase in diversity in onshore compared to offshore bears.The differences are most likely driven by differential exposure in the environment, such as to diet, contaminants and parasites, which are known to differ between the two groups. Such changes in microbiota may therefore have implications for health; nutrition, digestion and immunity.
Our work shows for the first time that global change driven alterations in habitat use are associated with changes in the gut microbiota composition and diversity of a free-ranging species. Understanding the ways in which polar bears respond to climate change mediated displacement from primary habitat is crucial in discerning their ability to cope with an increasingly changeable and uncertain environment. Considering that anthropogenic pressures on wildlife are abundant globally, this study highlights the need for more wildlife-microbiota work to assess the extent of this impact – especially for our most vulnerable and endangered species.
Sophie Watson is a PhD Researcher at Cardiff University who studies the effects of changing land use and parasite/contaminant profiles on the faecal microbiota of polar bears and wolverines. Sophie previously worked onblack bear and brown bear research projects in America and Canada, including the ‘USGS Northern Continental Divide Grizzly Bear Research Project’ in Montana and various projects throughout Alaska.
Watson et al.’s paper, ‘Global change-driven use of onshore habitat impacts polar bear faecal microbiota’, is published in The ISME Journal.