M. Bradley Hanson

• Northwest Fisheries Science Center

Highly social top marine predators, including many cetaceans, exhibit culturally learned ecological behaviours such as diet preference and foraging strategy that can affect their resilience to competition or anthropogenic impacts. When these species are also endangered, conservation efforts require management strategies based on a comprehensive und...

Understanding how the environment mediates an organism's ability to meet basic survival requirements is a fundamental goal of ecology. Vessel noise is a global threat to marine ecosystems and is increasing in intensity and spatiotemporal extent due to growth in shipping coupled with physical changes to ocean soundscapes from ocean warming and acidi...

Introduction Eastern Boundary Upwelling Systems are some of the most productive marine ecosystems in the world. Little is known about habitat associations and spatial distributions of marine predators during seasonal periods of low productivity because there are few at-sea surveys during this period. During low productivity or prey scarcity, predat...

Here we update U.S. West Coast Biologically Important Areas (BIAs) that were published in 2015 using new data and approaches. Additionally, BIAs were delineated for two species that were not delineated in the 2015 BIAs: fin whales and Southern Resident killer whales (SRKW). While harbor porpoise BIAs remained the same, substantial changes were made...

Endangered Southern Resident killer whales (Orcinus orca) are fish-eaters that preferentially prey on adult Chinook salmon (Oncorhynchus tshawytscha). Despite being salmon specialists, individuals from all three killer whale pods (J, K, L) have been observed harassing and killing porpoises (family Phocoenidae) without consuming them. Retrospectivel...

Using DNA methylation profiles (n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex...

Using DNA methylation profiles (n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex...

Aging, often considered a result of random cellular damage, can be accurately estimated using DNA methylation profiles, the foundation of pan-tissue epigenetic clocks. Here, we demonstrate the development of universal pan-mammalian clocks, using 11,754 methylation arrays from our Mammalian Methylation Consortium, which encompass 59 tissue types acr...

Photographic identification catalogs of individual killer whales (Orcinus orca) over time provide a tool for remote health assessment. We retrospectively examined digital photographs of Southern Resident killer whales in the Salish Sea to characterize skin changes and to determine if they could be an indicator of individual, pod, or population heal...

Epigenetic approaches for estimating the age of living organisms are revolutionizing studies of long-lived species. Molecular biomarkers that allow age estimates from small tissue biopsies promise to enhance studies of long-lived whales; addressing a fundamental and challenging parameter in wildlife management. DNA methylation (DNAm) can affect gen...

Understanding the factors that cause endangered populations to either grow or decline is crucial for preserving biodiversity. Conservation efforts often address extrinsic threats, such as environmental degradation and overexploitation, that can limit the recovery of endangered populations. Genetic factors such as inbreeding depression can also affe...

In cooperative species, human-induced rapid environmental change may threaten cost–benefit tradeoffs of group behavioral strategies that evolved in past environments. Capacity for behavioral flexibility can increase population viability in novel environments. Whether the partitioning of individual responsibilities within social groups is fixed or f...

The timing, or phenology, of predator activity in relation to their prey is critical for survival and fitness, yet rarely quantified for marine species, even those of conservation concern. We use a large database of professional and crowd-sourced observations analyzed with hierarchical spline occupancy models to quantify seasonal variation in occur...

The Pacific Offshore killer whale population is currently listed as data deficient on the IUCN Red List and Threatened in Canada. The population is estimated at 300 individuals with a range extending from Southern California to the Aleutian Islands in Alaska. Only 157 encounters with this ecotype have been photo-documented between 1988 and 2014; co...

Opportunities to assess odontocete health are restricted due to their limited time at the surface, relatively quick movements and large geographic ranges. For endangered populations such as the southern resident killer whales (SKRWs) of the northeast Pacific Ocean, taking advantage of non-invasive samples such as expelled mucus and exhaled breath i...

Studying patterns in marine mammal stranding cases can provide insight into changes in population health, abundance, and distribution. Cetaceans along the United States West coast strand for a wide variety of reasons, including disease, injury, and poor nutritional status, all of which may be caused by both natural and anthropogenic factors. Examin...

Cryptococcus gattii is a fungal pathogen that primarily affects the respiratory and nervous systems of humans and other animals. C. gattii emerged in temperate North America in 1999 as a multispecies outbreak of cryptococcosis in British Columbia (Canada) and Washington State and Oregon (USA), affecting humans, domestic animals, and wildlife. Here...

No PDF available ABSTRACT Killer whales face many anthropogenic threats including vessel traffic, noise, and reduced prey availability. Here, we use high-resolution suction-cup Dtags to study the behavior of endangered Southern Resident killer whales that rely on biosonar to hunt salmon, and investigate how proximate vessels affect foraging behavio...

No PDF available ABSTRACT Understanding ambient noise effects on foraging ecology of endangered killer whales is a necessary step toward predicting population-level consequences of acoustic disturbance. However, this has been limited by the difficulty of identifying prey capture which typically occurs out of sight, and by the challenge of obtaining...

No PDF available ABSTRACT Since 2006, a network of hydrophones has been deployed along the outer coasts of Washington, Oregon, and California to improve our understanding of endangered Southern Resident killer whale (SRKW) movements outside the inland waters of the Salish Sea and refine Critical Habitat designation. During this time period, improve...

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigate whether variation in killer whale (Orcinus o...

Vessel traffic is prevalent throughout marine environments. However, we often have a limited understanding of vessel impacts on marine wildlife, particularly cetaceans, due to challenges of studying fully-aquatic species. To investigate vessel and acoustic effects on cetacean foraging behavior, we attached suction-cup sound and movement tags to end...

Maximum lifespan of a species is the oldest that individuals can survive, reflecting the genetic limit of longevity in an ideal environment. Here we report methylation-based models that accurately predict maximum lifespan (r=0.89), gestational time (r=0.96), and age at sexual maturity (r=0.87), using cytosine methylation patterns collected from ove...

No PDF available ABSTRACT Southern Resident killer whales (SRKW) were listed as endangered in 2005, requiring designation of Critical Habitat. At that time little was known about SRKW distribution in winter/spring along the outer coast. From 2004 to 2016, we conducted nine winter/spring surveys aboard NOAA ocean-class vessels to locate and follow S...

Understanding diet is critical for conservation of endangered predators. Southern Resident killer whales (SRKW) (Orcinus orca) are an endangered population occurring primarily along the outer coast and inland waters of Washington and British Columbia. Insufficient prey has been identified as a factor limiting their recovery, so a clear understandin...

Harbor porpoise in the North Pacific are found in coastal waters from southern California to Japan, but population structure is poorly known outside of a few local areas. We used multiplexed amplicon sequencing of 292 loci and genotyped clusters of SNPs as microhaplotypes (N=271 samples) in addition to mtDNA sequence data (N=413 samples), to examin...

ABSTRACT Aging is often perceived as a degenerative process caused by random accrual of cellular damage over time. In spite of this, age can be accurately estimated by epigenetic clocks based on DNA methylation profiles from almost any tissue of the body. Since such pan-tissue epigenetic clocks have been successfully developed for several different...

Accurate knowledge of behavior is necessary to effectively manage the effects of human activities on wildlife, including vessel-based whale-watching. Yet, the wholly aquatic nature of cetaceans makes understanding their basic behavioral ecology quite challenging. An endangered population of killer whales faces several identified threats including p...

Understanding health and mortality in killer whales (Orcinus orca) is crucial for management and conservation actions. We reviewed pathology reports from 53 animals that stranded in the eastern Pacific Ocean and Hawaii between 2004 and 2013 and used data from 35 animals that stranded from 2001 to 2017 to assess association with morphometrics, blubb...

Anthropogenic activities that have negative consequences on foraging outcomes warrant special concern in endangered species. Prey availability and vessel disturbance are identified risk factors of endangered Southern Resident killer whales (SRKW) as vessels and associated sounds can mask echolocation signals used for foraging and/or disrupt foragin...

Understanding diet composition is fundamental to making conservation and management decisions about depleted species, particularly when nutritional stress is a potential threat hindering recovery. Diet in free-ranging marine mammals is challenging to study, but stable isotope mixing models are a powerful means of estimating the contribution of prey...

Primary fungal diseases in marine mammals are rare. Mucormycosis, a disease caused by fungi of the order Mucorales, has been documented in few cetaceans and pinnipeds. In 2012, the first case of mucormycosis in the Pacific Northwest was documented in a dead stranded harbor porpoise (Phocoena phocoena) in Washington state. Since then, mucormycosis h...

Competition for prey resources among ecologically similar populations that occur in sympatry can be reduced by spatiotemporal resource partitioning. Understanding patterns of habitat use of cetaceans can be difficult since they are highly mobile and can have large home ranges. We used passive acoustic monitoring at 15 sites along the coast of Washi...

It's the prey that matters Although many people think of dinosaurs as being the largest creatures to have lived on Earth, the true largest known animal is still here today—the blue whale. How whales were able to become so large has long been of interest. Goldbogen et al. used field-collected data on feeding and diving events across different types...

Foraging behavior in odontocetes is fundamentally tied to the use of sound. Resident-type killer whales use echolocation to locate and capture elusive salmonid prey. In this investigation, acoustic recording tags were suction cup-attached to endangered Southern Resident killer whales to describe their acoustic behavior during different phases of fo...

Behavioral data can be important for effective management of endangered marine predators, but can be challenging to obtain. We utilized suction cup-attached biologging tags equipped with stereo hydrophones, triaxial accelerometers, triaxial magnetometers, pressure and temperature sensors, to characterize the subsurface behavior of an endangered pop...

Through consultations with veterinarians and experts, NOAA Fisheries in the U.S. and Department of Fisheries and Oceans (DFO) in Canada worked closely with many partners and authorized an emergency response, which resulted in the first-ever attempt to provide veterinary care for a free-ranging SRKW (J50).

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree‐like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidat...

Studies of odontocete foraging ecology have been limited by the challenges of observing prey capture events and outcomes underwater. We sought to determine whether subsurface movement behavior recorded from archival tags could accurately identify foraging events by fish-eating killer whales. We used multisensor bio-logging tags attached by suction...

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidat...

Recent exploration into the interactions and relationship between hosts and their microbiota has revealed a connection between many aspects of the host's biology, health and associated microorganisms. Whereas amplicon sequencing has traditionally been used to characterise the microbiome, the increasing number of published population genomics datase...

Recent exploration into the interactions and relationship between hosts and their microbiota has revealed a connection between many aspects of the host’s biology, health and associated microorganisms. Whereas amplicon sequencing has traditionally been used to characterise the microbiome, the increasing number of published population genomics datase...

There are genetic risks associated with small population sizes, including loss of genetic diversity and inbreeding depression. The southern resident killer whale Orcinus orca population is a group of ~80 whales listed as ‘endangered’ under the U.S. Endangered Species Act. Recovery efforts are focused on increasing prey and reducing impacts from env...

We evaluated harbor porpoise (Phocoena phocoena (Linnaeus, 1758)) strandings in the Salish Sea to determine calving seasonality (1980–2015). A total of 443 strandings were analyzed, of which 134 were calves and 53 were neonates. Stranded calves were reported every month, but peaked in July, August, and September. Based on fetal size and an estimate...

In the Salish Sea, the endangered Southern Resident Killer Whale (SRKW) is a high trophic indicator of ecosystem health. Three major threats have been identified for this population: reduced prey availability, anthropogenic contaminants, and marine vessel disturbances. These perturbations can culminate in significant morbidity and mortality, usuall...

Many marine mammal predators, particularly pinnipeds, have increased in abundance in recent decades, generating new challenges for balancing human uses with recovery goals via ecosystem-based management. We used a spatio-temporal bioenergetics model of the Northeast Pacific Ocean to quantify how predation by three species of pinnipeds and killer wh...

Whale-watching is often conducted from motorized vessels, which contribute to underwater noise pollution and can disturb marine mammals. Protective measures can ameliorate some effects of disturbance but it is crucial to empirically assess effectiveness of such measures, particularly for endangered species. We quantitatively compared noise exposure...

Conflicts can arise when the recovery of one protected species limits the recovery of another through competition or predation. The recovery of many marine mammal populations on the west coast of the United States has been viewed as a success; however, within Puget Sound in Washington State, the increased abundance of three protected pinniped speci...

Killer whales are apex predators with diet specializations that vary among ecotypes. Resident killer whales use broadband echolocation clicks to detect and capture fish prey in their underwater environment. Here, we describe the echolocation behavior of endangered Southern Resident killer whales using DTAGs to determine subsurface foraging activity...

A prototype real-time, passive-acoustic observing system for killer whales was developed and tested off the coast of Newport, Oregon, USA. The system consists of two modules: 1) the passive-acoustic monitoring (PAM) module, which sits on the seafloor and continuously monitors the underwater soundscape for killer whale calls, and 2) a surface buoy,...

Analysing population genomic data from killer whale ecotypes, which we estimate have globally radiated within less than 250,000 years, we show that genetic structuring including the segregation of potentially functional alleles is associated with socially inherited ecological niche. Reconstruction of ancestral demographic history revealed bottlenec...

Details of fixed non-synonymous changes in the exons of protein coding genes, including the per-individual and per-population read count for each allele.

D-statistic (ABBA-BABA test) values and standard error estimates for the inference of ancient admixture.

Supplementary Figures 1-17, Supplementary Tables 1-10, Supplementary Note 1 and Supplementary References

Pairwise genetic distance estimates and 100 bootstrap replicates.

Pairwise relatedness estimates

Persistent organic pollutants (POPs), specifically PCBs, PBDEs, and DDTs, in the marine environment are well documented, however accumulation and mobilization patterns at the top of the food-web are poorly understood. This study broadens the understanding of POPs in the endangered Southern Resident killer whale population by addressing modulation b...

The interaction between ecology, culture and genome evolution remains poorly understood. Analysing population genomic data from killer whale ecotypes, which we estimate have globally radiated within less than 250,000 years, we show that genetic structuring including the segregation of potentially functional alleles is associated with socially inher...

Estimating diet composition is important for understanding interactions between predators and prey and thus illuminating ecosystem function. The diet of many species, however, is difficult to observe directly. Genetic analysis of fecal material collected in the field is therefore a useful tool for gaining insight into wild animal diets. In this stu...

Distance matrix of number of nucleotide differences among species in the baseline. (CSV)

Table of sampling dates and associated sample groups for the 175 fecal samples used in the analysis. (CSV)

Description of methods for estimated daily salmon abundance. (DOCX)

Alignment of the primer regions. (DOCX)

BLAST results of Pacific salmon 16s sequences from GenBank against our baseline. (CSV)

Whale watching has become increasingly popular as an ecotourism activity around the globe and is beneficial for environmental education and local economies. Southern Resident killer whales (Orcinus orca) comprise an endangered population that is frequently observed by a large whale watching fleet in the inland waters of Washington state and British...

Analysis of qualitative characteristics as factors. The qualitative vessel characteristics: type, orientation and propulsion system, were also analyzed as factors in the negative log likelihood model. (PDF)

Noise levels and average vessel length. There was no significant relationship between received noise levels (dB re 1 μPa) and average vessel length (m) per interval. Variation in average vessel length was skewed toward the smaller vessels. (TIF)

Noise levels and average vessel type. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel type per interval. Variation in average vessel type was heavily skewed toward inflatables and no intervals where vessels were on average of the medium or large hard bottom distinction. (TIF)

Average distance of vessels to tagged whales and average vessel type. The average distance (m) of vessels to tagged whales had a highly significant correlation with average vessel type per interval (F1, 55 = 27.77, p<0.001). (TIF)

Noise levels and average vessel orientation. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel orientation per interval. Orientation descriptions are relating the motor’s relationship to the whale (i.e. motor away indicates the motor is facing away from the whale, see Table 1). There was little...

Noise levels and average distance of vessels to tagged whales. There was no significant relationship between received noise levels (dB re 1 μPa) and the average distance of vessels to tagged whales (m) per interval. Variation in average vessel distance was slightly skewed toward closer distances. (TIF)

Average distance of vessels to tagged whales and average vessel length. The average distance (m) of vessels to tagged whales had a highly significant correlation with average vessel length (m) per interval (F1, 55 = 30.62, p<0.001). (TIF)

Average vessel length and average vessel type. The average vessel length (m) had a highly significant correlation with average vessel type per interval (F1, 55 = 67.47, p<0.001). (TIF)

Underlying data for analyses. Spreadsheet includes: whale and vessel locations, vessel characteristics, and received noise levels for all intervals in this study. (XLSX)

Noise levels and average propulsion system. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel propulsion system per interval. Variation in average vessel propulsion system was very poor with outboard motors present on most vessels per interval. (TIF)

Average number of propellers and average vessel speed. The average number of propellers had a marginally significant correlation with average vessel speed per interval (F1, 55 = 3.385, p = 0.071). (TIF)

AICc results of models with qualitative characteristics as factors. Negative log likelihood model results when vessel type, propulsion system and orientation were included as factors. The AICc value for the full model excluding research vessel-only intervals where each qualitative characteristic was assigned a numerical value (according to Table 1)...

Biologic sample collection in wild cetacean populations is challenging. Most information on toxicant levels is obtained from blubber biopsy samples; however, sample collection is invasive and strictly regulated under permit, thus limiting sample numbers. Methods are needed to monitor toxicant levels that increase temporal and repeat sampling of ind...

The primary prey species of mammal-eating killer whales in the Salish Sea, the inland waters of southern British Columbia and Washington state, have experienced dramatic increases in population abundances in the last 25 years. It is possible that changes in prey abundance over time have resulted in changes in predator spatial use, occurrence and gr...

Cephalopods are an important component of many cetacean diets. Although some odontocete species in the subfamily, which includes killer whales, primarily consume squid (e.g., pilot whales, beaked whales), killer whales, for the most part, are thought to specialize. In the North Pacific Ocean, three ecotypes have been identified based on dietary spe...

Using moored autonomous acoustic recorders to detect and record the vocalizations of social odonotocetes to determine their occurrence patterns is a non-invasive tool in the study of these species in remote locations. Acoustic recorders were deployed in seven locations on the continental shelf of the U.S. west coast from Cape Flattery, WA to Pt. Re...

In this investigation, acoustic tags (DTAGs) allow us to better understand noise exposure and potential behavioral effects in endangered Southern Resident killer whales (SRKWs). Designated critical habit of SRKWs includes summer foraging areas where vessel traffic from commercial shipping, whale-watching, and other boating activities is common. Ris...

Several different factors in the collection and preservation of whale skin and blubber samples were examined to determine their effect on the results obtained by stable nitrogen and carbon isotope (δ15N and δ13C) analysis. Samples of wet killer whale skin retained their original stable isotope values for up to 14 d at 4°C or lower. However, decompo...

Killer whales (Orcinus orca) are widely distributed throughout the world’s oceans, yet little has been documented about their stranding patterns. Knowledge of stranding patterns improves our ability to examine and sample carcasses and provides a foundation for understanding killer whale natural history, diet, reproduction, anthropogenic stressors,...