Genomic analyses reveal range-wide devastation of sea otter populations.

The genetic consequences of species-wide declines are rarely quantified because the timing and extent of the decline varies across the species' range. The sea otter (Enhydra lutris) is a unique model in this regard. Their dramatic decline from thousands to fewer than 100 individuals per population occurred range-wide and nearly simultaneously due to the 18th-19th century fur trade. Consequently, each sea otter population represents an independent natural experiment of recovery after extreme population decline. We designed sequence capture probes for 50 Mb of sea otter exonic and neutral genomic regions. We sequenced 107 sea otters from five populations that span the species range to high coverage (18-76×) and three historical Californian samples from ~1500 and ~200 years ago to low coverage (1.5-3.5×). We observe distinct population structure and find that sea otters in California are the last survivors of a divergent lineage isolated for thousands of years and therefore warrant special conservation concern. We detect signals of extreme population decline in every surviving sea otter population and use this demographic history to design forward-in-time simulations of coding sequence. Our simulations indicate that this decline could lower the fitness of recovering populations for generations. However, the simulations also demonstrate how historically low effective population sizes prior to the fur trade may have mitigated the effects of population decline on genetic health. Our comprehensive approach shows how demographic inference from genomic data, coupled with simulations, allows assessment of extinction risk and different models of recovery.

Human activities disturb haul out and nursing behavior of Pacific harbor seals at Punta Banda Estuary, Mexico.

Humans frequently interact with Pacific harbor seals (Phoca vitulina richardii) at Punta Banda Estuary, Baja California, Mexico, due to the high incidence of recreational activities people undertake there. The immediate effect of these interactions is that seals flush to the water, reducing their time on land and, probably, increasing their energy expenditure. On-land observations were used to study the impact of different sources of disturbance on seal behavior and evaluate their effect on the amount of time dedicated to nursing over three pupping seasons, (2015-2017), with 0.58-0.81 disturbance events/hour recorded over the entire sampling period. Terrestrial vehicles were the source with the highest disturbance rate (number of disturbance events/h), followed closely by pedestrians. However, the proportion of seals affected was highest when pedestrians were the disturbance source. Recovery events (seals hauling out after flushing) occurred after 34% of disturbance events, after less than half of which the same number of hauled-out seals as there were prior to the disturbance were observed. Recovery time varied among the years studied, of which 2017 saw the longest recovery time. In addition, pedestrians were the disturbance source with the longest recovery time. Given that resting on land is essential for pup survival, which depends on both the establishment of the mother-pup bond from birth and its maintenance throughout nursing, flushing behavior may have significant implications for the entire colony during the nursing season. We recorded a decrease in nursing duration, which did not return to the same level even after recovery and the resumption of nursing. Terrestrial vehicles were found to be the disturbance source that shortened nursing events most significantly.

Assessing Marine Endocrine-Disrupting Chemicals in the Critically Endangered California Condor: Implications for Reintroduction to Coastal Environments.

Coastal reintroduction sites for California condors (Gymnogyps californianus) can lead to elevated halogenated organic compound (HOC) exposure and potential health impacts due to the consumption of scavenged marine mammals. Using nontargeted analysis based on comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry (GC×GC/TOF-MS), we compared HOC profiles of plasma from inland and coastal scavenging California condors from the state of California (CA), and marine mammal blubber from CA and the Gulf of California off Baja California (BC), Mexico. We detected more HOCs in coastal condors (32 ± 5, mean number of HOCs ± SD, n = 7) than in inland condors (8 ± 1, n = 10) and in CA marine mammals (136 ± 87, n = 25) than in BC marine mammals (55 ± 46, n = 8). ∑DDT-related compounds, ∑PCBs, and total tris(chlorophenyl)methane (∑TCPM) were, respectively, ∼7, ∼3.5, and ∼148 times more abundant in CA than in BC marine mammals. The endocrine-disrupting potential of selected polychlorinated biphenyls (PCB) congeners, TCPM, and TCPMOH was determined by in vitro California condor estrogen receptor (ER) activation. The higher levels of HOCs in coastal condors compared to those in inland condors and lower levels of HOC contamination in Baja California marine mammals compared to those from the state of California are factors to consider in condor reintroduction efforts.

Trophic ecology of Mexican Pacific harbor seal colonies using carbon and nitrogen stable isotopes.

There is limited information that provides a comprehensive understanding of the trophic ecology of Mexican Pacific harbor seal (Phoca vitulina richardii) colonies. While scat analysis has been used to determine the diet of some colonies, the integrative characterization of its feeding habits on broader temporal and spatial scales remains limited. We examined potential feeding grounds, trophic niche width, and overlap, and inferred the degree of dietary specialization using stable carbon and nitrogen isotope ratios (δ13C and δ15N) in this subspecies. We analyzed δ13C and δ15N on fur samples from pups collected at five sites along the western coast of the Baja California Peninsula, Mexico. Fur of natal coat of Pacific harbor seal pups begins to grow during the seventh month in utero until the last stage of gestation. Therefore pup fur is a good proxy for the mother's feeding habits in winter (~December to March), based on the timing of gestation for the subspecies in this region. Our results indicated that the δ13C and δ15N values differed significantly among sampling sites, with the highest mean δ15N value occurring at the southernmost site, reflecting a well-characterized north to south latitudinal 15N-enrichment in the food web. The tendency identified in δ13C values, in which the northern colonies showed the most enriched values, suggests nearshore and benthic-demersal feeding habits. A low variance in δ13C and δ15N values for each colony (<1‰) and relatively small standard ellipse areas suggest a specialized foraging behavior in adult female Pacific harbor seals in Mexican waters.

The Pacific harbor seal gut microbiota in Mexico: Its relationship with diet and functional inferences.

Diet is a primary driver of the composition of gut microbiota and is considered one of the main routes of microbial colonization. Prey identification is fundamental for correlating the diet with the presence of particular microbial groups. The present study examined how diet influenced the composition and function of the gut microbiota of the Pacific harbor seal (Phoca vitulina richardii) in order to better understand the role of prey consumption in shaping its microbiota. This species is a good indicator of the quality of the local environment due to both its foraging and haul-out site fidelity. DNA was extracted from 20 fecal samples collected from five harbor seal colonies located in Baja California, Mexico. The V4 region of 16S rRNA gene was amplified and sequenced using the Illumina technology. Results showed that the gut microbiota of the harbor seals was dominated by the phyla Firmicutes (37%), Bacteroidetes (26%) and Fusobacteria (26%) and revealed significant differences in its composition among the colonies. Funtional analysis using the PICRUSt software suggests a high number of pathways involved in the basal metabolism, such as those for carbohydrates (22%) and amino acids (20%), and those related to the degradation of persistent environmental pollutants. In addition, a DNA metabarcoding analysis of the same samples, via the amplification and sequencing of the mtRNA 16S and rRNA 18S genes, was used to identify the prey consumed by harbor seals revealing the consumption of prey with mainly demersal habits. Functional redundancy in the seal gut microbiota was observed, irrespective of diet or location. Our results indicate that the frequency of occurrence of specific prey in the harbor seal diet plays an important role in shaping the composition of the gut microbiota of harbor seals by influencing the relative abundance of specific groups of gut microorganisms. A significant relationship was found among diet, gut microbiota composition and OTUs assigned to a particular metabolic pathway.

Do marine reserves increase prey for California sea lions and Pacific harbor seals?

Community marine reserves are geographical areas closed to fishing activities, implemented and enforced by the same fishermen that fish around them. Their main objective is to recover commercial stocks of fish and invertebrates. While marine reserves have proven successful in many parts of the world, their success near important marine predator colonies, such as the California sea lion (Zalophus californianus) and the Pacific harbor seal (Phoca vitulina richardii), is yet to be analyzed. In response to the concerns expressed by local fishermen about the impact of the presence of pinnipeds on their communities' marine reserves, we conducted underwater surveys around four islands in the Pacific west of the Baja California Peninsula: two without reserves (Todos Santos and San Roque); one with a recently established reserve (San Jeronimo); and, a fourth with reserves established eight years ago (Natividad). All these islands are subject to similar rates of exploitation by fishing cooperatives with exclusive rights. We estimated fish biomass and biodiversity in the seas around the islands, applying filters for potential California sea lion and harbor seal prey using known species from the literature. Generalized linear mixed models revealed that the age of the reserve has a significant positive effect on fish biomass, while the site (inside or outside of the reserve) did not, with a similar result found for the biomass of the prey of the California sea lion. Fish biodiversity was also higher around Natividad Island, while invertebrate biodiversity was higher around San Roque. These findings indicate that marine reserves increase overall fish diversity and biomass, despite the presence of top predators, even increasing the numbers of their potential prey. Community marine reserves may help to improve the resilience of marine mammals to climate-driven phenomena and maintain a healthy marine ecosystem for the benefit of both pinnipeds and fishermen.

Eco-Evolutionary Processes Generating Diversity Among Bottlenose Dolphin, Tursiops truncatus, Populations off Baja California, Mexico.

For highly mobile species that nevertheless show fine-scale patterns of population genetic structure, the relevant evolutionary mechanisms determining structure remain poorly understood. The bottlenose dolphin (Tursiops truncatus) is one such species, exhibiting complex patterns of genetic structure associated with local habitat dependence in various geographic regions. Here we studied bottlenose dolphin populations in the Gulf of California and Pacific Ocean off Baja California where habitat is highly structured to test associations between ecology, habitat dependence and genetic differentiation. We investigated population structure at a fine geographic scale using both stable isotope analysis (to assess feeding ecology) and molecular genetic markers (to assess population structure). Our results show that there are at least two factors affecting population structure for both genetics and feeding ecology (as indicated by stable isotope profiles). On the one hand there is a signal for the differentiation of individuals by ecotype, one foraging more offshore than the other. At the same time, there is differentiation between the Gulf of California and the west coast of Baja California, meaning that for example, nearshore ecotypes were both genetically and isotopically differentiated either side of the peninsula. We discuss these data in the context of similar studies showing fine-scale population structure for delphinid species in coastal waters, and consider possible evolutionary mechanisms.

California sea lions (Zalophus californianus californianus) have lower chlorinated hydrocarbon contents in northern Baja California, México, than in California, USA.

Chlorinated hydrocarbons (CHs) were determined in blubber samples of 18 California sea lions (Zalophus californianus californianus) that stranded dead along Todos Santos Bay, Ensenada, Baja California, México, January 2000-November 2001. Summation operatorDDTs were the dominant group (geometric mean 3.8 microg/g lipid weight), followed by polychlorinated biphenyls ( summation operatorPCBs, 2.96 microg/g), chlordanes (0.12 microg/g) and hexachlorocyclohexanes (0.06 microg/g). The summation operatorDDTs/ summation operatorPCBs ratio was 1.3. We found CH levels more than one order of magnitude lower than those reported for California sea lion samples collected along the California coast, USA, during the same period as our study. This sharp north-south gradient suggests that Z. californianus stranded in Ensenada (most of them males) would probably have foraged during the summer near rookeries 500-1000 km south of Ensenada and the rest of the year migrate northwards, foraging along the Baja California peninsula, including Ensenada, and probably farther north.