Genomics of post-bottleneck recovery in the northern elephant seal.

Populations and species are threatened by human pressure, but their fate is variable. Some depleted populations, such as that of the northern elephant seal (Mirounga angustirostris), recover rapidly even when the surviving population was small. The northern elephant seal was hunted extensively and taken by collectors between the early 1800s and 1892, suffering an extreme population bottleneck as a consequence. Recovery was rapid and now there are over 200,000 individuals. We sequenced 260 modern and 8 historical northern elephant seal nuclear genomes to assess the impact of the population bottleneck on individual northern elephant seals and to better understand their recovery. Here we show that inbreeding, an increase in the frequency of alleles compromised by lost function, and allele frequency distortion, reduced the fitness of breeding males and females, as well as the performance of adult females on foraging migrations. We provide a detailed investigation of the impact of a severe bottleneck on fitness at the genomic level and report on the role of specific gene systems.

Estimating population size when individuals are asynchronous: A model illustrated with northern elephant seal breeding colonies.

Our aim was to develop a method for estimating the number of animals using a single site in an asynchronous species, meaning that not all animals are present at once so that no one count captures the entire population. This is a common problem in seasonal breeders, and in northern elephant seals, we have a model for quantifying asynchrony at the Año Nuevo colony. Here we test the model at several additional colonies having many years of observations and demonstrate how it can account for animals not present on any one day. This leads to correction factors that yield total population from any single count throughout a season. At seven colonies in California for which we had many years of counts of northern elephant seals, we found that female arrival date varied < 2 days between years within sites and by < 5 days between sites. As a result, the correction factor for any one day was consistent, and at each colony, multiplying a female count between 26 and 30 Jan by 1.15 yielded an estimate of total population size that minimized error. This provides a method for estimating the female population size at colonies not yet studied. Our method can produce population estimates with minimal expenditure of time and resources and will be applicable to many seasonal species with asynchronous breeding phenology, particularly colonial birds and other pinnipeds. In elephant seals, it will facilitate monitoring the population over its entire range.

The rise and fall of dialects in northern elephant seals.

Vocal dialects are fundamental to our understanding of the transmission of social behaviours between individuals and populations, however few accounts trace this phenomenon among mammals over time. Northern elephant seals (Mirounga angustirostris) provide a rare opportunity to examine the trajectory of dialects in a long-lived mammalian species. Dialects were first documented in the temporal patterns of the stereotyped vocal displays produced by breeding males at four sites in the North Pacific in 1968 and 1969, as the population recovered from extreme exploitation. We evaluated the longevity of these geographical differences by comparing these early recordings to calls recently recorded at these same locations. While the presence of vocal dialects in the original recordings was re-confirmed, geographical differences in vocal behaviour were not found at these breeding rookeries nearly 50 years later. Moreover, the calls of contemporary males displayed more structural complexity after approximately four generations, with substantial between-individual variation and call features not present in the historical data. In the absence of measurable genetic variation in this species-owing to an extreme population bottleneck-a combination of migration patterns and cultural mutation are proposed as factors influencing the fall of dialects and the dramatic increase in call diversity.

Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast.

Northern elephant seals (Mirounga angustirostris) are characterized by extended fasting during which they rely entirely on their own body reserves. During fasts, lipids are mobilized from blubber to match the energy requirements of the animal. This transfer frees toxic fat-soluble pollutants into the blood circulation, which may exert adverse health effects, especially in young and developing animals. We investigated the dynamics of mobilization of polychlorinated biphenyls (PCBs) from the blubber of northern elephant seal pups during the post-weaning fast. Longitudinal samples of blubber and serum were collected from free-ranging animals throughout the fast at Año Nuevo, California. Blubber biopsies were separated into inner and outer layers. The PCB profiles of blubber and serum consisted mainly of penta- (PCB-101, -110, -118), hexa- (PCB-138, -153) and hepta- (PCB-180, -183, -187) chlorobiphenyls, which accounted for almost 90% of the total PCB burden. Total PCB concentrations in inner blubber increased significantly between early and late fasting (563.6+/-162.0 microg/kg lipids at early versus 911.6+/-513.1 microg/kg lipids at late fasting) whereas they remained fairly constant in outer blubber (572.6+/-134.8 microg/kg lipids at early versus 659.2+/-158.8 microg/kg lipids at late fasting). A corresponding rise of PCB concentrations was observed in serum during the second half of the fast (3.8+/-1.1 microg/l serum at early versus 7.2+/-0.9 microg/l at late fasting). The longitudinal changes in circulating total PCBs could not be explained by the changes in serum lipid fractions (cholesterol, phospholipids, triacylglycerols and free fatty acids). The increases in total PCB concentrations in inner blubber and serum were more pronounced in leaner animals, which suggests that they might be more at risk to potential toxic effects.

Mating system and reproductive success in eastern Pacific harbour seals.

Harbour seals sometimes breed along inland travel corridors where females become clustered in space and time and males establish underwater acoustic display territories similar to terrestrial arenas known as resource-based leks. Under these conditions, we predicted that higher levels of polygyny would be observed than has been previously reported for this species mating in open coast environments without travel corridors. Reproductive success (RS) of 70 males was measured using 20 microsatellite DNA loci and likelihood-based paternity analysis of 136 offspring collected over 3 years. Most males were assigned either zero or one paternity with 80% confidence. The greatest number of pups assigned to one male in a season was two. Variance in RS was higher for males than females (which are biologically limited to one offspring per year) indicating low to mild polygyny. In addition, distributions of relatedness values among pups within year classes did not differ significantly from a simulated distribution with R = 0, indicating that half-siblings were uncommon. Overall, polygyny levels were low relative to terrestrial pinniped mating systems and similar to observations from a harbour seal population along an open coast. Due to large confidence intervals associated with our results, we cannot rule out the hypothesis that a travel corridor might increase the degree of polygyny skew relative to that observed in open coast environments. Habitat appeared to influence male strategies as the most successful males in open coast environments patrolled offshore, while the most successful male in this study defended a territory along the travel corridor.

Ocean climate and seal condition.

BACKGROUND: The condition of many marine mammals varies with fluctuations in productivity and food supply in the ocean basin where they forage. Prey is impacted by physical environmental variables such as cyclic warming trends. The weaning weight of northern elephant seal pups, Mirounga angustirostris, being closely linked to maternal condition, indirectly reflects prey availability and foraging success of pregnant females in deep waters of the northeastern Pacific. The aim of this study was to examine the effect of ocean climate on foraging success in this deep-diving marine mammal over the course of three decades, using cohort weaning weight as the principal metric of successful resource accrual. RESULTS: The mean annual weaning weight of pups declined from 1975 to the late 1990s, a period characterized by a large-scale, basin-wide warm decadal regime that included multiple strong or long-duration El Niños; and increased with a return to a cool decadal regime from about 1999 to 2004. Increased foraging effort and decreased mass gain of adult females, indicative of reduced foraging success and nutritional stress, were associated with high ocean temperatures. CONCLUSION: Despite ranging widely and foraging deeply in cold waters beyond coastal thermoclines in the northeastern Pacific, elephant seals are impacted significantly by ocean thermal dynamics. Ocean warming redistributes prey decreasing foraging success of females, which in turn leads to lower weaning mass of pups. Annual fluctuations in weaning mass, in turn, reflect the foraging success of females during the year prior to giving birth and signals changes in ocean temperature cycles.

Polychlorinated biphenyls, dioxins, and furans in weaned, free-ranging northern elephant seal pups from central California, USA.

The aim of this study was to measure persistent organic pollutants in northern elephant seals ([NES], Mirounga angustirotris). We obtained blubber biopsy samples from six healthy, newly weaned NES pups from Año Nuevo, California (USA). Contaminant levels were lower than those of other pinnipeds studied on the west coast of North America. Blubber concentrations of polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans averaged 700 +/- 130 microg/kg, 32 +/- 23 ng/kg, and 17 +/- 5 ng/kg (lipid wt), respectively. These contaminants originate from transplacental transfer and from maternal milk, which, in turn, reflect contaminants acquired by the mother from prey during long-distance foraging trips in the northeastern Pacific Ocean. The PCB profile in the blubber of NES pups mainly was composed of penta-, hexa-, and hepta-chlorobiphenyls, possibly reflecting the deep-sea nature of the mother's diet. Our results suggest that NES pups, in contrast to pups of other pinnipeds in the eastern Pacific Ocean, are exposed to low levels of persistent organic pollutants, reflecting an open ocean signal.

PCBs and DDT in the serum of juvenile California sea lions: associations with vitamins A and E and thyroid hormones.

Top-trophic predators like California sea lions bioaccumulate high levels of persistent fat-soluble pollutants that may provoke physiological impairments such as endocrine or vitamins A and E disruption. We measured circulating levels of polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethane (DDT) in 12 healthy juvenile California sea lions captured on Año Nuevo Island, California, in 2002. We investigated the relationship between the contamination by PCBs and DDT and the circulating levels of vitamins A and E and thyroid hormones (thyroxine, T4 and triiodothyronine, T3). Serum concentrations of total PCBs (sigmaPCBs) and total DDT were 14 +/- 9 mg/kg and 28 +/- 19 mg/kg lipid weight, respectively. PCB toxic equivalents (sigmaPCB TEQs) were 320 +/- 170 ng/kg lipid weight. Concentrations of sigmaPCBs and sigmaPCB TEQs in serum lipids were negatively correlated (p < 0.05) with serum vitamin A and T3, potentially reflecting PCB-related toxicity. A slight but not significant negative correlation (p < 0.1) was observed between serum T4 and the levels of sigmaPCBs and sigmaPCB TEQs. Conversely, no relationship was evident between the contaminant concentrations and vitamin E (p > 0.1). As juvenile California sea lions are useful sentinels of coastal contamination, the high levels encountered in their serum is cause for concern about the ecosystem health of the area.

The effect of a low-frequency sound source (acoustic thermometry of the ocean climate) on the diving behavior of juvenile northern elephant seals, Mirounga angustirostris.

Changes in the diving behavior of individual free-ranging juvenile northern elephant seals, Mirounga angustirostris, exposed to the acoustic thermometry of the ocean climate (ATOC) sound source were examined using data loggers. Data loggers were attached to the animals and measured swim speed, maximum depth of dive, dive duration, surface interval, descent and ascent rate, and descent and ascent angle along with sound pressure level (SPL). The ATOC sound source was at a depth of 939 m and transmitted at 195 dB re: 1 microPa at 1 m centered at 75 Hz with a 37.5-Hz bandwidth. Sound pressure levels (SPL) measured at the seal during transmissions averaged 128 dB and ranged from 118 to 137 dB re: 1 microPa for the 60-90 Hz band, in comparison to ambient levels of 87-107 dB within this band. In no case did an animal end its dive or show any other obvious change in behavior upon exposure to the ATOC sound. Subtle changes in diving behavior were detected, however. During exposure, deviations in descent rate were greater than 1 s.d. of the control mean in 9 of 14 seals. Dive depth increased and descent velocity increased in three animals, ascent velocity decreased in two animals, ascent rate increased in one animal and decreased in another, and dive duration decreased in only one animal. There was a highly significant positive correlation between SPL and descent rate. The biological significance of these subtle changes is likely to be minimal. This is the first study to quantify behavioral responses of an animal underwater with simultaneous measurements of SPL of anthropogenic sounds recorded at the animal.

Organochlorine pollutants [corrected] in California sea lions revisited.

BACKGROUND: Dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCBs) are ubiquitous environmental contaminants that have been banned in most countries, but considerable amounts continue to cycle the ecosphere. Top trophic level predators, like sea birds and marine mammals, bioaccumulate these lipophilic compounds, reflecting their presence in the environment. RESULTS: We measured concentrations of tDDT (p,p' - DDT + p,p' - DDD + p,p' - DDE) and PCBs in the blubber of dead California sea lions stranded along the California coast. tDDT and PCB concentrations were 150 +/- 257 ug/g lipid weight (mean +/- SD) and 44 +/- 78 ug/g lipid weight, respectively. There were no differences in tDDT or PCB concentrations between animal categories varying in sex or age. There was a trend towards a decrease in tDDT and PCB concentrations from northern to southern California. The lipid content of the blubber was negatively correlated with levels of tDDT and PCBs. tDDT concentrations were approximately 3 times higher than PCB concentrations. CONCLUSIONS: tDDT levels in the blubber of California sea lions decreased by over one order of magnitude from 1970 to 2000. PCB level changes over time were unclear owing to a paucity of data and analytical differences over the years. Current levels of these pollutants in California sea lions are among the highest among marine mammals and exceed those reported to cause immunotoxicity or endocrine disruption.

Expanded niche for white sharks.

Until the advent of electronic tagging technology, the inherent difficulty of studying swift and powerful marine animals made ecological information about sharks of the family Lamnidae difficult to obtain. Here we report the tracking of movements of white sharks by using pop-up satellite archival tags, which reveal that their migratory movements, depth and ambient thermal ranges are wider than was previously thought.