Ecological correlates of blue whale movement behavior and its predictability in the California Current Ecosystem during the summer-fall feeding season.

BACKGROUND: Species distribution models have shown that blue whales (Balaenoptera musculus) occur seasonally in high densities in the most biologically productive regions of the California Current Ecosystem (CCE). Satellite telemetry studies have additionally shown that blue whales in the CCE regularly switch between behavioral states consistent with area-restricted searching (ARS) and transiting, indicative of foraging in and moving among prey patches, respectively. However, the relationship between the environmental correlates that serve as a proxy of prey relative to blue whale movement behavior has not been quantitatively assessed. METHODS: We investigated the association between blue whale behavioral state and environmental predictors in the coastal environments of the CCE using a long-term satellite tracking data set (72 tagged whales; summer-fall months 1998-2008), and predicted the likelihood of ARS behavior at tracked locations using nonparametric multiplicative regression models. The models were built using data from years of cool, productive conditions and validated against years of warm, low-productivity conditions. RESULTS: The best model contained four predictors: chlorophyll-a, sea surface temperature, and seafloor aspect and depth. This model estimated highest ARS likelihood (> 0.8) in areas with high chlorophyll-a levels (> 0.65 mg/m3), intermediate sea surface temperatures (11.6-17.5 °C), and shallow depths (< 850 m). Overall, the model correctly predicted behavioral state throughout the coastal environments of the CCE, while the validation indicated an ecosystem-wide reduction in ARS likelihood during warm years, especially in the southern portion. For comparison, a spatial coordinates model (longitude × latitude) performed slightly better than the environmental model during warm years, providing further evidence that blue whales exhibit strong foraging site fidelity, even when conditions are not conducive to successful foraging. CONCLUSIONS: We showed that blue whale behavioral state in the CCE was predictable from environmental correlates and that ARS behavior was most prevalent in regions of known high whale density, likely reflecting where large prey aggregations consistently develop in summer-fall. Our models of whale movement behavior enhanced our understanding of species distribution by further indicating where foraging was more likely, which could be of value in the identification of key regions of importance for endangered species in management considerations. The models also provided evidence that decadal-scale environmental fluctuations can drive shifts in the distribution and foraging success of this blue whale population.

Memory and resource tracking drive blue whale migrations.

In terrestrial systems, the green wave hypothesis posits that migrating animals can enhance foraging opportunities by tracking phenological variation in high-quality forage across space (i.e., "resource waves"). To track resource waves, animals may rely on proximate cues and/or memory of long-term average phenologies. Although there is growing evidence of resource tracking in terrestrial migrants, such drivers remain unevaluated in migratory marine megafauna. Here we present a test of the green wave hypothesis in a marine system. We compare 10 years of blue whale movement data with the timing of the spring phytoplankton bloom resulting in increased prey availability in the California Current Ecosystem, allowing us to investigate resource tracking both contemporaneously (response to proximate cues) and based on climatological conditions (memory) during migrations. Blue whales closely tracked the long-term average phenology of the spring bloom, but did not track contemporaneous green-up. In addition, blue whale foraging locations were characterized by low long-term habitat variability and high long-term productivity compared with contemporaneous measurements. Results indicate that memory of long-term average conditions may have a previously underappreciated role in driving migratory movements of long-lived species in marine systems, and suggest that these animals may struggle to respond to rapid deviations from historical mean environmental conditions. Results further highlight that an ecological theory of migration is conserved across marine and terrestrial systems. Understanding the drivers of animal migration is critical for assessing how environmental changes will affect highly mobile fauna at a global scale.

Fin whale movements in the Gulf of California, Mexico, from satellite telemetry.

Fin whales (Balaenoptera physalus) have a global distribution, but the population inhabiting the Gulf of California (GoC) is thought to be geographically and genetically isolated. However, their distribution and movements are poorly known. The goal of this study was to describe fin whale movements for the first time from 11 Argos satellite tags deployed in the southwest GoC in March 2001. A Bayesian Switching State-Space Model was applied to obtain improved locations and to characterize movement behavior as either "area-restricted searching" (indicative of patch residence, ARS) or "transiting" (indicative of moving between patches). Model performance was assessed with convergence diagnostics and by examining the distribution of the deviance and the behavioral parameters from Markov Chain Monte Carlo models. ARS was the predominant mode behavior 83% of the time during both the cool (December-May) and warm seasons (June-November), with slower travel speeds (mean = 0.84 km/h) than during transiting mode (mean = 3.38 km/h). We suggest ARS mode indicates either foraging activities (year around) or reproductive activities during the winter (cool season). We tagged during the cool season, when the whales were located in the Loreto-La Paz Corridor in the southwestern GoC, close to the shoreline. As the season progressed, individuals moved northward to the Midriff Islands and the upper gulf for the warm season, much farther from shore. One tag lasted long enough to document a whale's return to Loreto the following cool season. One whale that was originally of undetermined sex, was tagged in the Bay of La Paz and was photographed 10 years later with a calf in the nearby San Jose Channel, suggesting seasonal site fidelity. The tagged whales moved along the western GoC to the upper gulf seasonally and did not transit to the eastern GoC south of the Midriff Islands. No tagged whales left the GoC, providing supporting evidence that these fin whales are a resident population.

The political biogeography of migratory marine predators.

During their migrations, marine predators experience varying levels of protection and face many threats as they travel through multiple countries' jurisdictions and across ocean basins. Some populations are declining rapidly. Contributing to such declines is a failure of some international agreements to ensure effective cooperation by the stakeholders responsible for managing species throughout their ranges, including in the high seas, a global commons. Here we use biologging data from marine predators to provide quantitative measures with great potential to inform local, national and international management efforts in the Pacific Ocean. We synthesized a large tracking data set to show how the movements and migratory phenology of 1,648 individuals representing 14 species-from leatherback turtles to white sharks-relate to the geopolitical boundaries of the Pacific Ocean throughout species' annual cycles. Cumulatively, these species visited 86% of Pacific Ocean countries and some spent three-quarters of their annual cycles in the high seas. With our results, we offer answers to questions posed when designing international strategies for managing migratory species.

Demography or selection on linked cultural traits or genes? Investigating the driver of low mtDNA diversity in the sperm whale using complementary mitochondrial and nuclear genome analyses.

Mitochondrial DNA has been heavily utilized in phylogeography studies for several decades. However, underlying patterns of demography and phylogeography may be misrepresented due to coalescence stochasticity, selection, variation in mutation rates and cultural hitchhiking (linkage of genetic variation to culturally-transmitted traits affecting fitness). Cultural hitchhiking has been suggested as an explanation for low genetic diversity in species with strong social structures, counteracting even high mobility, abundance and limited barriers to dispersal. One such species is the sperm whale, which shows very limited phylogeographic structure and low mtDNA diversity despite a worldwide distribution and large population. Here, we use analyses of 175 globally distributed mitogenomes and three nuclear genomes to evaluate hypotheses of a population bottleneck/expansion vs. a selective sweep due to cultural hitchhiking or selection on mtDNA as the mechanism contributing to low worldwide mitochondrial diversity in sperm whales. In contrast to mtDNA control region (CR) data, mitogenome haplotypes are largely ocean-specific, with only one of 80 shared between the Atlantic and Pacific. Demographic analyses of nuclear genomes suggest low mtDNA diversity is consistent with a global reduction in population size that ended approximately 125,000 years ago, correlated with the Eemian interglacial. Phylogeographic analysis suggests that extant sperm whales descend from maternal lineages endemic to the Pacific during the period of reduced abundance and have subsequently colonized the Atlantic several times. Results highlight the apparent impact of past climate change, and suggest selection and hitchhiking are not the sole processes responsible for low mtDNA diversity in this highly social species.

The development of an intermediate-duration tag to characterize the diving behavior of large whales.

The development of high-resolution archival tag technologies has revolutionized our understanding of diving behavior in marine taxa such as sharks, turtles, and seals during their wide-ranging movements. However, similar applications for large whales have lagged behind due to the difficulty of keeping tags on the animals for extended periods of time. Here, we present a novel configuration of a transdermally attached biologging device called the Advanced Dive Behavior (ADB) tag. The ADB tag contains sensors that record hydrostatic pressure, three-axis accelerometers, magnetometers, water temperature, and light level, all sampled at 1 Hz. The ADB tag also collects Fastloc GPS locations and can send dive summary data through Service Argos, while staying attached to a whale for typical periods of 3-7 weeks before releasing for recovery and subsequent data download. ADB tags were deployed on sperm whales (Physeter macrocephalus; N = 46), blue whales (Balaenoptera musculus; N = 8), and fin whales (B. physalus; N = 5) from 2007 to 2015, resulting in attachment durations from 0 to 49.6 days, and recording 31 to 2,539 GPS locations and 27 to 2,918 dives per deployment. Archived dive profiles matched well with published dive shapes of each species from short-term records. For blue and fin whales, feeding lunges were detected using peaks in accelerometer data and matched corresponding vertical excursions in the depth record. In sperm whales, rapid orientation changes in the accelerometer data, often during the bottom phase of dives, were likely related to prey pursuit, representing a relative measure of foraging effort. Sperm whales were documented repeatedly diving to, and likely foraging along, the seafloor. Data from the temperature sensor described the vertical structure of the water column in all three species, extending from the surface to depths >1,600 m. In addition to providing information needed to construct multiweek time budgets, the ADB tag is well suited to studying the effects of anthropogenic sound on whales by allowing for pre- and post-exposure monitoring of the whale's dive behavior. This tag begins to bridge the gap between existing long-duration but low-data throughput tags, and short-duration, high-resolution data loggers.

Critically endangered western gray whales migrate to the eastern North Pacific.

Western North Pacific gray whales (WGWs), once considered extinct, are critically endangered with unknown migratory routes and reproductive areas. We attached satellite-monitored tags to seven WGWs on their primary feeding ground off Sakhalin Island, Russia, three of which subsequently migrated to regions occupied by non-endangered eastern gray whales (EGWs). A female with the longest-lasting tag visited all three major EGW reproductive areas off Baja California, Mexico, before returning to Sakhalin Island the following spring. Her 22 511 km round-trip is the longest documented mammal migration and strongly suggests that some presumed WGWs are actually EGWs foraging in areas historically attributed to WGWs. The observed migration routes provide evidence of navigational skills across open water that break the near-shore north-south migratory paradigm of EGWs. Despite evidence of genetic differentiation, these tagging data indicate that the population identity of whales off Sakhalin Island needs further evaluation.

Spatial and temporal occurrence of blue whales off the U.S. West Coast, with implications for management.

Mortality and injuries caused by ship strikes in U.S. waters are a cause of concern for the endangered population of blue whales (Balaenoptera musculus) occupying the eastern North Pacific. We sought to determine which areas along the U.S. West Coast are most important to blue whales and whether those areas change inter-annually. Argos-monitored satellite tags were attached to 171 blue whales off California during summer/early fall from 1993 to 2008. We analyzed portions of the tracks that occurred within U.S. Exclusive Economic Zone waters and defined the 'home range' (HR) and 'core areas' (CAU) as the 90% and 50% fixed kernel density distributions, respectively, for each whale. We used the number of overlapping individual HRs and CAUs to identify areas of highest use. Individual HR and CAU sizes varied dramatically, but without significant inter-annual variation despite covering years with El Niño and La Niña conditions. Observed within-year differences in HR size may represent different foraging strategies for individuals. The main areas of HR and CAU overlap among whales were near highly productive, strong upwelling centers that were crossed by commercial shipping lanes. Tagged whales generally departed U.S. Exclusive Economic Zone waters from mid-October to mid-November, with high variability among individuals. One 504-d track allowed HR and CAU comparisons for the same individual across two years, showing similar seasonal timing, and strong site fidelity. Our analysis showed how satellite-tagged blue whales seasonally used waters off the U.S. West Coast, including high-risk areas. We suggest possible modifications to existing shipping lanes to reduce the likelihood of collisions with vessels.

Kinship of long-term associates in the highly social sperm whale.

The evolution of stable social groups can be promoted by both indirect and direct fitness benefits. Sperm whales (Physeter macrocephalus) are highly social, with a hierarchical social structure based around core groups of adult females and subadults, a rare level of complexity among mammals. We combined long-term satellite tracking (ranging from 11 to 607 days) of 51 individual sperm whales with genetic kinship analysis to assess the pattern of kin associations within and among coherent social units. Unlike findings for other species with similar social structure, we find no consistent correlation between kinship and association apart from close associations between two pairs of first-order relatives. A third pair of first-order relatives did not associate, and overall, the mean relatedness was the same within as among social groups. However, social behaviour can also be promoted by ecological factors such as resource dispersion. We assessed putative foraging behaviour during travel from the satellite-tracking data, which suggested that prey resources were dispersed and unpredictable, a condition that could promote living in groups.