Behavioral responses across a mosaic of ecosystem states restructure a sea otter-urchin trophic cascade.

Consumer and predator foraging behavior can impart profound trait-mediated constraints on community regulation that scale up to influence the structure and stability of ecosystems. Here, we demonstrate how the behavioral response of an apex predator to changes in prey behavior and condition can dramatically alter the role and relative contribution of top-down forcing, depending on the spatial organization of ecosystem states. In 2014, a rapid and dramatic decline in the abundance of a mesopredator (Pycnopodia helianthoides) and primary producer (Macrocystis pyrifera) coincided with a fundamental change in purple sea urchin (Strongylocentrotus purpuratus) foraging behavior and condition, resulting in a spatial mosaic of kelp forests interspersed with patches of sea urchin barrens. We show that this mosaic of adjacent alternative ecosystem states led to an increase in the number of sea otters (Enhydra lutris nereis) specializing on urchin prey, a population-level increase in urchin consumption, and an increase in sea otter survivorship. We further show that the spatial distribution of sea otter foraging efforts for urchin prey was not directly linked to high prey density but rather was predicted by the distribution of energetically profitable prey. Therefore, we infer that spatially explicit sea otter foraging enhances the resistance of remnant forests to overgrazing but does not directly contribute to the resilience (recovery) of forests. These results highlight the role of consumer and predator trait-mediated responses to resource mosaics that are common throughout natural ecosystems and enhance understanding of reciprocal feedbacks between top-down and bottom-up forcing on the regional stability of ecosystems.

Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters✰.

Harmful algal blooms produce toxins that bioaccumulate in the food web and adversely affect humans, animals, and entire marine ecosystems. Blooms of the diatom Pseudo-nitzschia can produce domoic acid (DA), a toxin that most commonly causes neurological disease in endothermic animals, with cardiovascular effects that were first recognized in southern sea otters. Over the last 20 years, DA toxicosis has caused significant morbidity and mortality in marine mammals and seabirds along the west coast of the USA. Identifying DA exposure has been limited to toxin detection in biological fluids using biochemical assays, yet measurement of systemic toxin levels is an unreliable indicator of exposure dose or timing. Furthermore, there is little information regarding repeated DA exposure in marine wildlife. Here, the association between long-term environmental DA exposure and fatal cardiac disease was investigated in a longitudinal study of 186 free-ranging sea otters in California from 2001 - 2017, highlighting the chronic health effects of a marine toxin. A novel Bayesian spatiotemporal approach was used to characterize environmental DA exposure by combining several DA surveillance datasets and integrating this with life history data from radio-tagged otters in a time-dependent survival model. In this study, a sea otter with high DA exposure had a 1.7-fold increased hazard of fatal cardiomyopathy compared to an otter with low exposure. Otters that consumed a high proportion of crab and clam had a 2.5- and 1.2-times greater hazard of death due to cardiomyopathy than otters that consumed low proportions. Increasing age is a well-established predictor of cardiac disease, but this study is the first to identify that DA exposure affects the risk of cardiomyopathy more substantially in prime-age adults than aged adults. A 4-year-old otter with high DA exposure had 2.3 times greater risk of fatal cardiomyopathy than an otter with low exposure, while a 10-year old otter with high DA exposure had just 1.2 times greater risk. High Toxoplasma gondii titers also increased the hazard of death due to heart disease 2.4-fold. Domoic acid exposure was most detrimental for prime-age adults, whose survival and reproduction are vital for population growth, suggesting that persistent DA exposure will likely impact long-term viability of this threatened species. These results offer insight into the pervasiveness of DA in the food web and raise awareness of under-recognized chronic health effects of DA for wildlife at a time when toxic blooms are on the rise.

Wild sea otter mussel pounding leaves archaeological traces.

Wild sea otters (Enhydra lutris) are the only marine mammals that habitually use stones while foraging, using them to break open hard-shelled foods like marine snails and bivalves. However, the physical effects of this behavior on local environments are unknown. We show that sea otters pounding mussels on tidally emergent rocks leave distinct material traces, which can be recognized using methods from archaeology. We observed sea otters pounding mussels at the Bennett Slough Culverts site, California, USA, over a l0-year period. Sea otters repeatedly used the same rocks as anvils, which resulted in distinctive wear patterns on the rocks and accumulations of broken mussel shells, all fractured in a characteristic way, below them. Our results raise the potential for discovery of similar sea otter pounding sites in areas that no longer have resident sea otter populations.

Limb-use by foraging marine turtles, an evolutionary perspective.

The use of limbs for foraging is documented in both marine and terrestrial tetrapods. These behaviors were once believed to be less likely in marine tetrapods due to the physical constraints of body plans adapted to locomotion in a fluid environment. Despite these obstacles, ten distinct types of limb-use while foraging have been previously reported in nine marine tetrapod families. Here, we expand the types of limb-use documented in marine turtles and put it in context with the diversity of marine tetrapods currently known to use limbs for foraging. Additionally, we suggest that such behaviors could have occurred in ancestral turtles, and thus, possibly extend the evolutionary timeline of limb-use behavior in marine tetrapods back approximately 70 million years. Through direct observation in situ and crowd-sourcing, we document the range of behaviors across habitats and prey types, suggesting its widespread occurrence. We argue the presence of these behaviors among marine tetrapods may be limited by limb mobility and evolutionary history, rather than foraging ecology or social learning. These behaviors may also be remnant of ancestral forelimb-use that have been maintained due to a semi-aquatic life history.

Mitogenomes and relatedness do not predict frequency of tool-use by sea otters.

Many ecological aspects of tool-use in sea otters are similar to those in Indo-Pacific bottlenose dolphins. Within an area, most tool-using dolphins share a single mitochondrial haplotype and are more related to each other than to the population as a whole. We asked whether sea otters in California showed similar genetic patterns by sequencing mitogenomes of 43 otters and genotyping 154 otters at 38 microsatellite loci. There were six variable sites in the mitogenome that yielded three haplotypes, one found in only a single individual. The other two haplotypes contained similar percentages (33 and 36%) of frequent tool-users and a variety of diet types. Microsatellite analyses showed that snail specialists, the diet specialist group that most frequently used tools, were no more related to each other than to the population as a whole. The lack of genetic association among tool-using sea otters compared with dolphins may result from the length of time each species has been using tools. Tool-use in dolphins appears to be a relatively recent innovation (less than 200 years) but sea otters have probably been using tools for many thousands or even millions of years.