Decadal-scale phenology and seasonal climate drivers of migratory baleen whales in a rapidly warming marine ecosystem.

Species' response to rapid climate change can be measured through shifts in timing of recurring biological events, known as phenology. The Gulf of Maine is one of the most rapidly warming regions of the ocean, and thus an ideal system to study phenological and biological responses to climate change. A better understanding of climate-induced changes in phenology is needed to effectively and adaptively manage human-wildlife conflicts. Using data from a 20+ year marine mammal observation program, we tested the hypothesis that the phenology of large whale habitat use in Cape Cod Bay has changed and is related to regional-scale shifts in the thermal onset of spring. We used a multi-season occupancy model to measure phenological shifts and evaluate trends in the date of peak habitat use for North Atlantic right (Eubalaena glacialis), humpback (Megaptera novaeangliae), and fin (Balaenoptera physalus) whales. The date of peak habitat use shifted by +18.1 days (0.90 days/year) for right whales and +19.1 days (0.96 days/year) for humpback whales. We then evaluated interannual variability in peak habitat use relative to thermal spring transition dates (STD), and hypothesized that right whales, as planktivorous specialist feeders, would exhibit a stronger response to thermal phenology than fin and humpback whales, which are more generalist piscivorous feeders. There was a significant negative effect of western region STD on right whale habitat use, and a significant positive effect of eastern region STD on fin whale habitat use indicating differential responses to spatial seasonal conditions. Protections for threatened and endangered whales have been designed to align with expected phenology of habitat use. Our results show that whales are becoming mismatched with static seasonal management measures through shifts in their timing of habitat use, and they suggest that effective management strategies may need to alter protections as species adapt to climate change.

Gross and histopathologic diagnoses from North Atlantic right whale Eubalaena glacialis mortalities between 2003 and 2018.

Seventy mortalities of North Atlantic right whales Eubalaena glacialis (NARW) were documented between 2003 and 2018 from Florida, USA, to the Gulf of St. Lawrence, Canada. These included 29 adults, 14 juveniles, 10 calves, and 17 of unknown age class. Females represented 65.5% (19/29) of known-sex adults. Fourteen cases had photos only; 56 carcasses received external examinations, 44 of which were also necropsied. Cause of death was determined in 43 cases, of which 38 (88.4%) were due to anthropogenic trauma: 22 (57.9%) from entanglement, and 16 (42.1%) from vessel strike. Gross and histopathologic lesions associated with entanglement were often severe and included deep lacerations caused by constricting line wraps around the flippers, flukes, and head/mouth; baleen plate mutilation; chronic extensive bone lesions from impinging line, and traumatic scoliosis resulting in compromised mobility in a calf. Chronically entangled whales were often in poor body condition and had increased cyamid burden, reflecting compromised health. Vessel strike blunt force injuries included skull and vertebral fractures, blubber and muscle contusions, and large blood clots. Propeller-induced wounds often caused extensive damage to blubber, muscle, viscera, and bone. Overall prevalence of NARW entanglement mortalities increased from 21% (1970-2002) to 51% during this study period. This demonstrates that despite mitigation efforts, entanglements and vessel strikes continue to inflict profound physical trauma and suffering on individual NARWs. These cumulative mortalities are also unsustainable at the population level, so urgent and aggressive intervention is needed to end anthropogenic mortality in this critically endangered species.

Forgotten Mediterranean calving grounds of grey and North Atlantic right whales: evidence from Roman archaeological records.

Right whales (Eubalaena glacialis) were extirpated from the eastern North Atlantic by commercial whaling. Grey whales (Eschrichtius robustus) disappeared from the entire North Atlantic in still-mysterious circumstances. Here, we test the hypotheses that both species previously occurred in the Mediterranean Sea, an area not currently considered part of their historical range. We used ancient DNA barcoding and collagen fingerprinting methods to taxonomically identify a rare set of 10 presumed whale bones from Roman and pre-Roman archaeological sites in the Strait of Gibraltar region, plus an additional bone from the Asturian coast. We identified three right whales, and three grey whales, demonstrating that the ranges of both of these species historically encompassed the Gibraltar region, probably including the Mediterranean Sea as calving grounds. Our results significantly extend the known range of the Atlantic grey whale, and suggest that 2000 years ago, right and grey whales were common when compared with other whale species. The disappearance of right and grey whales from the Mediterranean region is likely to have been accompanied by broader ecosystem impacts, including the disappearance of their predators (killer whales) and a reduction in marine primary productivity. The evidence that these two coastal and highly accessible species were present along the shores of the Roman Empire raises the hypothesis that they may have formed the basis of a forgotten whaling industry.

Prolonged particulate chromate exposure does not inhibit homologous recombination repair in North Atlantic right whale (Eubalaena glacialis) lung cells.

Chromosome instability is a common feature of cancers that forms due to the misrepair of DNA double strand breaks. Homologous recombination (HR) repair is a high fidelity DNA repair pathway that utilizes a homologous DNA sequence to accurately repair such damage and protect the genome. Prolonged exposure (>72h) to the human lung carcinogen, particulate hexavalent chromium (Cr(VI)), inhibits HR repair, resulting in increased chromosome instability in human cells. Comparative studies have shown acute Cr(VI) exposure induces less chromosome damage in whale cells than human cells, suggesting investigating the effect of this carcinogen in other species may inform efforts to prevent Cr(VI)-induced chromosome instability. Thus, the goal of this study was to determine the effect of prolonged Cr(VI) exposure on HR repair and clastogenesis in North Atlantic right whale (Eubalaena glacialis) lung cells. We show particulate Cr(VI) induces HR repair activity after both acute (24h) and prolonged (120h) exposure in North Atlantic right whale cells. Although the RAD51 response was lower following prolonged Cr(VI) exposure compared to acute exposure, the response was sufficient for HR repair to occur. In accordance with active HR repair, no increase in Cr(VI)-induced clastogenesis was observed with increased exposure time. These results suggest prolonged Cr(VI) exposure affects HR repair and genomic stability differently in whale and human lung cells. Future investigation of the differences in how human and whale cells respond to chemical carcinogens may provide valuable insight into mechanisms of preventing chemical carcinogenesis.

Expert Elicitation of Population-Level Effects of Disturbance.

Expert elicitation is a rigorous method for synthesizing expert knowledge to inform decision making and is reliable and practical when field data are limited. We evaluated the feasibility of applying expert elicitation to estimate population-level effects of disturbance on marine mammals. Diverse experts estimated parameters related to mortality and sublethal injury of North Atlantic right whales (Eubalaena glacialis). We are now eliciting expert knowledge on the movement of right whales among geographic regions to parameterize a spatial model of health. Expert elicitation complements methods such as simulation models or extrapolations from other species, sometimes with greater accuracy and less uncertainty.

Characterization of class I- and class II-like major histocompatibility complex loci in pedigrees of North Atlantic right whales.

North Atlantic right whales have one of the lowest levels of genetic variation at minisatellite loci, microsatellite loci, and mitochondrial control region haplotypes among mammals. Here, adaptive variation at the peptide binding region of class I and class II DRB-like genes of the major histocompatibility complex was assessed. Amplification of a duplicated region in 222 individuals revealed at least 11 class II alleles. Six alleles were assigned to the locus Eugl-DRB1 and 5 alleles were assigned to the locus Eugl-DRB2 by assessing segregation patterns of alleles from 81 parent/offspring pedigrees. Pedigree analysis indicated that these alleles segregated into 12 distinct haplotypes. Genotyping a smaller subset of unrelated individuals (n = 5 and 10, respectively) using different primer sets revealed at least 2 class II pseudogenes (with ≥ 4 alleles) and at least 3 class I loci (with ≥ 6 alleles). Class II sequences were significantly different from neutrality at peptide binding sites suggesting loci may be under the influence of balancing selection. Trans-species sharing of alleles was apparent for class I and class II sequences. Characterization of class II loci represents the first step in determining the relationship between major histocompatibility complex variability and factors affecting health and reproduction in this species.

Effects of inbreeding on reproductive success in endangered North Atlantic right whales.

Only approximately 356 North Atlantic right whales (Eubalaena glacialis) remain. With extremely low levels of genetic diversity, limited options for mates, and variation in reproductive success across females, there is concern regarding the potential for genetic limitations of population growth from inbreeding depression. In this study, we quantified reproductive success of female North Atlantic right whales with a modified de-lifing approach using reproductive history information collected over decades of field observations. We used double-digest restriction site-associated sequencing to sequence approximately 2% of the genome of 105 female North Atlantic right whales and combined genomic inbreeding estimates with individual fecundity values to assess evidence of inbreeding depression. Inbreeding depression could not explain the variance in reproductive success of females, however we present evidence that inbreeding depression may be affecting the viability of inbred fetuses-potentially lowering the reproductive success of the species as a whole. Combined, these results allay some concerns that genetic factors are impacting species survival as genetic diversity is being retained through selection against inbred fetuses. While still far fewer calves are being born each year than expected, the small role of genetics underlying variance in female fecundity suggests that variance may be explained by external factors that can potentially be mitigated through protection measures designed to reduce serious injury and mortality from human activities.

Feeling for food: Can rostro-mental hair arrays sense hydrodynamic cues for foraging North Atlantic right whales?

North Atlantic right whales (NARWs; Eubalaena glacialis) possess an arrangement of fine hairs on the rostrum and chin that may be used for hydrodynamic sensing during feeding. These hairs occur across mysticete species and are known to possess adequate innervation in the subdermal follicle to support their consideration as sensory hairs (vibrissae). However, the small size of the hair structure with respect to the enormous scale of the animal's body has caused doubts regarding their utility and prompted speculation that the hairs may be vestigial or minimally functional. Here we show that NARW hairs occur in abundance on the leading surface of the head in a unique and characteristic arrangement. We consider the sensory hairs in context of the fluid environment in which this species forages and argue that the size of the hair is scaled to the size of the animal's small planktonic prey, thus suggesting that the hairs play an important role in the sensory ecology of these animals.

Recommended metrics for quantifying underwater noise impacts on North Atlantic right whales.

Anthropogenic underwater noise has been identified as a potentially serious stressor for the critically endangered North Atlantic right whale (NARW). The Government of Canada is undertaking steps to better characterize the noise sources of most concern and their associated impacts, but there is currently an insufficient understanding of which noise sources are most impacting NARW in their Canadian habitat. This knowledge gap together with the myriad possible methods and metrics for quantifying underwater noise presents a confounding and challenging problem that risks delaying timely mitigation. This study presents the results from a 2020 workshop aimed at developing a series of metrics recommended specifically for better characterizing the types of noise deemed of greatest concern for NARW in Canadian waters. The recommendations provide a basis for more targeted research on noise impacts and set the stage for more effective management and protection of NARW, with potential conservation applications to similar species.

An overview of North Atlantic right whale acoustic behavior, hearing capabilities, and responses to sound.

Creating a baseline understanding of communicative signals and perceptual abilities is imperative for gaining insight into a species' life history. This is especially relevant for at-risk species, as it can aid in monitoring and conservation efforts. Marine mammals communicate predominately through acoustic modalities for a variety of functions, including foraging and reproduction. The acoustic signals produced by marine mammals, and their ability to perceive signals produced by conspecifics, are directly impacted by the level of ambient noise in the underwater environment in which they inhabit. Modern ocean noise levels are considerably louder than historical levels, and noise is therefore considered to be a threat to acoustically communicating marine mammal species. This review summarizes the documented acoustic signals, hearing abilities, and responses to sound of a critically endangered baleen whale, the North Atlantic right whale (Eubalaena glacialis), highlights gaps in the current body of literature, and identifies priorities for future research.

Stress and reproductive events detected in North Atlantic right whale blubber using a simplified hormone extraction protocol.

As studies quantifying steroid hormones in marine mammal blubber progress, methodological refinements may improve the utility and consistency of blubber hormone measurements. This study advances blubber extraction methodologies by testing a simplified extraction protocol that reduces time and complexity compared to a protocol widely used in cetacean blubber studies. Using blubber samples archived from remote biopsy (n = 21 live whales) and necropsy collection (n = 7 dead whales) of North Atlantic right whales (NARW; Eubalaena glacialis) of known life history states, we performed analytical and biological validations to assess the feasibility of measuring reproductive (testosterone, progesterone) and glucocorticoid (cortisol) hormones in blubber via enzyme immunoassay following the simplified extraction. Analytical validations (parallelism, accuracy, extraction efficiency, repeatability) showed the simplified extraction produced similar results to the extended protocol, offering a more efficient and consistent technique. In live, apparently healthy whales, blubber testosterone concentrations (mean ± SE) were significantly higher in males (2.02 ± 0.36 ng/g) compared to females (0.81 ± 0.15 ng/g). Blubber progesterone was highest in a confirmed pregnant female (60.3 ng/g), which was 12-fold greater than the mean concentration of non-pregnant females (4.56 ± 0.88 ng/g). Blubber cortisol concentrations in whales that died from anthropogenic causes averaged 5.31 ± 2.28 ng/g, whereas most live, healthy whales had cortisol values below 1 ng/g. Among living whales, a whale actively entangled in fishing gear had the highest blubber cortisol measurement (3.51 ng/g), exhibiting levels similar to whales that died from acute entanglement (2.88 ± 0.42 ng/g). Overall, the highest blubber cortisol concentration (18.0 ng/g) was measured in a dead whale with a severe chronic entanglement, approximately 30-fold greater than mean blubber cortisol of apparently healthy whales (0.58 ± 0.11 ng/g). The methodological approach presented here provides a reference for researchers interested in an alternative, streamlined technique for hormone extraction of cetacean blubber and contributes to the diverse tool set for stress and reproductive assessments of endangered NARWs.

The right whale mandatory ship reporting system: a retrospective.

In 1998, the United States sought and received International Maritime Organization-endorsement of two Mandatory Ship Reporting (MSR) systems designed to improve mariner awareness about averting ship collisions with the endangered North Atlantic right whale (Eubalaena glacialis). Vessel collisions are a serious threat to the right whale and the program was among the first formal attempts to reduce this threat. Under the provisions of the MSR, all ships >300 gross tons are required to report their location, speed, and destination to a shore-based station when entering two key right whale habitats: one in waters off New England and one off coastal Georgia and Florida. In return, reporting ships receive an automatically-generated message, delivered directly to the ship's bridge, that provides information about right whale vulnerability to vessel collisions and actions mariners can take to avoid collisions. The MSR has been in operation continuously from July 1999 to the present. Archived incoming reports provided a 15-plus year history of ship operations in these two locations. We analyzed a total of 26,772 incoming MSR messages logged between July 1999 and December 2013. Most ships that were required to report did so, and compliance rates were generally constant throughout the study period. Self-reported vessel speeds when entering the systems indicated that most ships travelled between 10 and 16 (range = 5-20 +) knots. Ship speeds generally decreased in 2009 to 2013 following implementation of vessel speed restrictions. The number of reports into the southern system remained relatively constant following a steady increase through 2007, but numbers in the northern system decreased annually beginning in 2008. If reporting is indicative of long-term patterns in shipping operations, it reflects noteworthy changes in marine transportation. Observed declines in ship traffic are likely attributable to the 2008-2009 economic recession, the containerized shipping industry making increased use of larger ships that made fewer trips, and diminished oil/gas US imports as previously inaccessible domestic deposits were exploited. Recent declines in shipping activity likely resulted in lowered collision risks for right whales and reduced their exposure to underwater noise from ships.