Effect of kelp gull harassment on southern right whale calf survival: a long-term capture-recapture analysis.

Kelp gulls (Larus dominicanus) commonly feed on the skin and blubber of surfacing southern right whales (SRW, Eubalaena australis) in the near shore waters of Península Valdés (PV), Argentina. Mothers and especially calves respond to gull attacks by changing their swimming speeds, resting postures and overall behaviour. Gull-inflicted wounds per calf have increased markedly since the mid-1990s. Unusually high mortality of young calves occurred locally after 2003, and increasing evidence points to gull harassment as a factor contributing to the excess deaths. After leaving PV, calves undertake a long migration with their mothers to summer feeding areas; their health during this strenuous exertion is likely to affect their probabilities of first-year survival. To explore the effects of gull-inflicted wounds on calf survival, we analysed 44 capture-recapture observations between 1974 and 2017, for 597 whales photo-identified in their years of birth between 1974 and 2011. We found a marked decrease in first-year survival associated with an increase in wound severity over time. Our analysis supports recent studies indicating that gull harassment at PV may impact SRW population dynamics.

Long-term stability in the circumpolar foraging range of a Southern Ocean predator between the eras of whaling and rapid climate change.

Assessing environmental changes in Southern Ocean ecosystems is difficult due to its remoteness and data sparsity. Monitoring marine predators that respond rapidly to environmental variation may enable us to track anthropogenic effects on ecosystems. Yet, many long-term datasets of marine predators are incomplete because they are spatially constrained and/or track ecosystems already modified by industrial fishing and whaling in the latter half of the 20th century. Here, we assess the contemporary offshore distribution of a wide-ranging marine predator, the southern right whale (SRW, Eubalaena australis), that forages on copepods and krill from ~30°S to the Antarctic ice edge (>60°S). We analyzed carbon and nitrogen isotope values of 1,002 skin samples from six genetically distinct SRW populations using a customized assignment approach that accounts for temporal and spatial variation in the Southern Ocean phytoplankton isoscape. Over the past three decades, SRWs increased their use of mid-latitude foraging grounds in the south Atlantic and southwest (SW) Indian oceans in the late austral summer and autumn and slightly increased their use of high-latitude (>60°S) foraging grounds in the SW Pacific, coincident with observed changes in prey distribution and abundance on a circumpolar scale. Comparing foraging assignments with whaling records since the 18th century showed remarkable stability in use of mid-latitude foraging areas. We attribute this consistency across four centuries to the physical stability of ocean fronts and resulting productivity in mid-latitude ecosystems of the Southern Ocean compared with polar regions that may be more influenced by recent climate change.

Optimizing hormone extraction protocols for whale baleen: Tackling questions of solvent:sample ratio and variation.

Obtaining endocrine data from alternative sample types such as baleen and other keratinized tissues has proven a valuable tool to investigate reproductive and stress physiology via steroid hormone quantification, and metabolic stress via thyroid hormone quantification in whales and other vertebrates. These alternative sample types provide an integrated measure of plasma levels over the period that the structure was growing, thus capturing months or even years of an individual's endocrine history. Additionally, their robust and stable keratin matrix allows such samples to be stored for years to decades, enabling the analysis and comparison of endocrine patterns from past and modern populations. However, the extraction and analysis of hormones from baleen and other keratinized tissues remains novel and requires both biological and analytical validations to ensure the method fulfills the requirements for its intended use. We utilized baleen recovered at necropsy from southern right whales (Eubalaena australis) that died at Península Valdés, Argentina, using a commercially available progesterone enzyme immunoassay (EIA) to address two methodological questions: 1) what is the minimum sample mass required to reliably quantify hormone content of baleen samples analyzed with commercially available EIAs, and 2) what is the optimal ratio of solvent volume to sample mass, i.e., the ratio that yields the maximum amount of hormone with high accuracy and low variability between replicates. We concluded that masses of at least 20 mg should be used whenever possible, and extraction is best performed using an 80:1 ratio of solvent to sample (volume of solvent to sample mass; µl:mg). These results can help researchers to make informed methodological decisions when using a destructive extraction method with rare or unique specimens.

Ocean warming threatens southern right whale population recovery.

Whales contribute to marine ecosystem functioning, and they may play a role in mitigating climate change and supporting the Antarctic krill (Euphausia superba) population, a keystone prey species that sustains the entire Southern Ocean (SO) ecosystem. By analyzing a five-decade (1971­2017) data series of individual southern right whales (SRWs; Eubalaena australis) photo-identified at Península Valdés, Argentina, we found a marked increase in whale mortality rates following El Niño events. By modeling how the population responds to changes in the frequency and intensity of El Niño events, we found that such events are likely to impede SRW population recovery and could even cause population decline. Such outcomes have the potential to disrupt food-web interactions in the SO, weakening that ecosystem's contribution to the mitigation of climate change at a global scale.

Retrospective analysis of the lifetime endocrine response of southern right whale calves to gull wounding and harassment: A baleen hormone approach.

Physiological measurements are informative in assessing the relative importance of stressors that potentially impact the health of wildlife. Kelp Gulls, Larus dominicanus (KG), resident to the region of Península Valdés, Argentina, have developed a unique behavior of landing on the backs of southern right whale adults and calves, Eubalaena australis (SRW), where they feed on their skin and blubber. This parasitic behavior results in large open wounds on the dorsal surface of the whale. Coincidently, the SRW population off the coast of Península Valdés has experienced elevated calf mortality. We quantified levels of glucocorticoids and thyroid hormone extracted from baleen of dead calves to evaluate, retrospectively, the endocrine response of whale calves to gull wounding and harassment. Baleen accumulates hormones as it grows, allowing evaluation of long-term trends in physiological condition. While glucocorticoids (GCs) are known to increase in response to stressors such as disturbance, the metabolic hormone triiodothyronine (T3) has been shown to decrease under sustained food deprivation but is largely unaffected by disturbance stress. We quantified lifetime patterns of GCs and T3 in baleen recovered at necropsy from 36 southern right whale calves with varying severity of wounding from KGs. GC levels in baleen correlated positively with the degree of wounding, while T3 levels remained stable irrespective of the severity of the wounding. Our results suggest no evidence of malnutrition in low vs. severely wounded whales. However, the positive correlation of GCs with wound severity indicates that heavily wounded calves are suffering high levels of physiological stress before they die. This suggests that KG wounding may have contributed to the high southern right whale calf mortality observed in the Península Valdés region of Argentina.

Symbiotic microbes and potential pathogens in the intestine of dead southern right whale (Eubalaena australis) calves.

Between 2003 and 2017, at least 706 southern right whale (Eubalaena australis) calves died at the Península Valdés calving ground in Argentina. Pathogenic microbes are often suggested to be the cause of stranding events in cetaceans; however, to date there is no evidence supporting bacterial infections as a leading cause of right whale calf deaths in Argentina. We used high-throughput sequencing and culture methods to characterize the bacterial communities and to detect potential pathogens from the intestine of stranded calves. We analyzed small and large intestinal contents from 44 dead calves that stranded at Península Valdés from 2005 to 2010 and found 108 bacterial genera, most identified as Firmicutes or Bacteroidetes, and 9 genera that have been previously implicated in diseases of marine mammals. Only one operational taxonomic unit was present in all samples and identified as Clostridium perfringens type A. PCR results showed that all C. perfringens isolates (n = 38) were positive for alpha, 50% for beta 2 (n = 19) and 47% for enterotoxin (CPE) genes (n = 18). The latter is associated with food-poisoning and gastrointestinal diseases in humans and possibly other animals. The prevalence of the cpe gene found in the Valdés' calves is unusually high compared with other mammals. However, insufficient histologic evidence of gastrointestinal inflammation or necrosis (the latter possibly masked by autolysis) in the gut of stranded calves, and absence of enterotoxin detection precludes conclusions about the role of C. perfringens in calf deaths. Further work is required to determine whether C. perfringens or other pathogens detected in this study are causative agents of calf deaths at Península Valdés.

The recovery of North Atlantic right whales, Eubalaena glacialis, has been constrained by human-caused mortality.

North Atlantic right whales (NARW), Eubalaena glacialis, were nearly exterminated by historical whaling. Their abundance slowly increased up until 2010, to a maximum of fewer than 500 whales, and since then they have been in decline. We assessed the extent to which the relatively slow increase demonstrated by NARW was intrinsic, and how much could be due to anthropogenic impacts. In order to do so, we first compared calf counts of three populations of Southern right whales (SRW), E. australis, with that of NARW, over the period 1992-2016. By this index, the annual rate of increase of NARW was approximately one-third of that of SRW. Next we constructed a population projection model for female NARW, using the highest annual survival estimates available from recent mark-resight analysis, and assuming a four-year calving interval. The model results indicated an intrinsic rate of increase of 4% per year, approximately twice that observed, and that adult female mortality is the main factor influencing this rate. Necropsy records demonstrate that anthropogenic mortality is the primary cause of known mortality of NARW. Anthropogenic mortality and morbidity has limited the recovery of NARW, and baseline conditions prior to their recent decline were already jeopardizing NARW recovery.

Lifetime glucocorticoid profiles in baleen of right whale calves: potential relationships to chronic stress of repeated wounding by Kelp Gulls.

Baleen tissue accumulates stress hormones (glucocorticoids, GC) as it grows, along with other adrenal, gonadal and thyroid hormones. The hormones are deposited in a linear fashion such that a single plate of baleen allows retrospective assessment and evaluation of long-term trends in the whales' physiological condition. In whale calves, a single piece of baleen contains hormones deposited across the lifespan of the animal, with the tip of the baleen representing prenatally grown baleen. This suggests that baleen recovered from stranded carcasses of whale calves could be used to examine lifetime patterns of stress physiology. Here we report lifetime profiles of cortisol and corticosterone in baleen of a North Atlantic right whale ('NARW'-Eubalaena glacialis) calf that died from a vessel strike, as well as four southern right whale ('SRW'-Eubalaena australis) calves that were found dead with varying severity of chronic wounding from Kelp Gull (Larus dominicanus) attacks. In all five calves, prenatally grown baleen exhibited a distinctive profile of elevated glucocorticoids that declined shortly before birth, similar to GC profiles reported from baleen of pregnant females. After birth, GC profiles in calf baleen corresponded with the degree of wounding. The NARW calf and two SRW calves with no or few gull wounds had relatively low and constant GC content throughout life, while two SRW calves with high numbers of gull wounds had pronounced elevations in baleen GC content in postnatal baleen followed by a precipitous decline shortly before death, a profile suggestive of prolonged chronic stress. Baleen samples may present a promising and valuable tool for defining the baseline physiology of whale calves and may prove useful for addressing conservation-relevant questions such as distinguishing acute from chronic stress and, potentially, determining cause of death.

Lateralization of mother-infant interactions in a diverse range of mammal species.

Left-cradling bias is a distinctive feature of maternal behaviour in humans and great apes, but its evolutionary origin remains unknown. In 11 species of marine and terrestrial mammal, we demonstrate consistent patterns of lateralization in mother-infant interactions, indicating right hemisphere dominance for social processing. In providing clear evidence that lateralized positioning is beneficial in mother-infant interactions, our results illustrate a significant impact of lateralization on individual fitness.

Cellular and ultrastructural characterization of the grey-morph phenotype in southern right whales (Eubalaena australis).

Southern right whales (SRWs, Eubalena australis) are polymorphic for an X-linked pigmentation pattern known as grey morphism. Most SRWs have completely black skin with white patches on their bellies and occasionally on their backs; these patches remain white as the whale ages. Grey morphs (previously referred to as partial albinos) appear mostly white at birth, with a splattering of rounded black marks; but as the whales age, the white skin gradually changes to a brownish grey color. The cellular and developmental bases of grey morphism are not understood. Here we describe cellular and ultrastructural features of grey-morph skin in relation to that of normal, wild-type skin. Melanocytes were identified histologically and counted, and melanosomes were measured using transmission electron microscopy. Grey-morph skin had fewer melanocytes when compared to wild-type skin, suggesting reduced melanocyte survival, migration, or proliferation in these whales. Grey-morph melanocytes had smaller melanosomes relative to wild-type skin, normal transport of melanosomes to surrounding keratinocytes, and normal localization of melanin granules above the keratinocyte nuclei. These findings indicate that SRW grey-morph pigmentation patterns are caused by reduced numbers of melanocytes in the skin, as well as by reduced amounts of melanin production and/or reduced sizes of mature melanosomes. Grey morphism is distinct from piebaldism and albinism found in other species, which are genetic pigmentation conditions resulting from the local absence of melanocytes, or the inability to synthesize melanin, respectively.

Post-mortem findings in southern right whales Eubalaena australis at Península Valdés, Argentina, 2003-2012.

Between 2003 and 2012, 605 southern right whales (SRW; Eubalaena australis) were found dead along the shores of Península Valdés (PV), Argentina. These deaths included alarmingly high annual losses between 2007 and 2012, a peak number of deaths (116) in 2012, and a significant number of deaths across years in calves-of-the-year (544 of 605 [89.9%]; average = 60.4 yr(-1)). Post-mortem examination and pathogen testing were performed on 212 whales; 208 (98.1%) were calves-of-the-year and 48.0% of these were newborns or neonates. A known or probable cause of death was established in only a small number (6.6%) of cases. These included ship strike in a juvenile and blunt trauma or lacerations (n = 5), pneumonia (n = 4), myocarditis (n = 2), meningitis (n = 1), or myocarditis and meningitis (n = 1) in calves. Ante-mortem gull parasitism was the most common gross finding. It was associated with systemic disease in a single 1-2 mo old calf. Immunohistochemical labeling for canine distemper virus, Toxoplasma gondii and Brucella spp., and PCR for cetacean morbillivirus (CeMV), influenza A, and apicomplexan protozoa were negative on formalin-fixed, paraffin-embedded lung and brain samples from a subset of whales; PCR for Brucella spp. was positive in a newborn/neonate with pneumonia. Skin samples from whales with gull parasitism were PCR negative for CeMV, poxvirus, and papillomavirus. This is the first long-term study to investigate and summarize notable post-mortem findings in the PV SRW population. Consistent, significant findings within or between years to explain the majority of deaths and those in high-mortality years remain to be identified.

Increased Wounding of Southern Right Whale (Eubalaena australis) Calves by Kelp Gulls (Larus dominicanus) at Península Valdés, Argentina.

At least 626 southern right whale (Eubalaena australis) calves died at the Península Valdés calving ground, Argentina, between 2003 and 2014. Intense gull harassment may have contributed to these deaths. In the 1970s, Kelp Gulls (Larus dominicanus) began feeding on skin and blubber pecked from the backs of living right whales at Valdés. The frequency of gull attacks has increased dramatically over the last three decades and mother-calf pairs are the primary targets. Pairs attacked by gulls spend less time nursing, resting and playing than pairs not under attack. In successive attacks, gulls open new lesions on the whales' backs or enlarge preexisting ones. Increased wounding could potentially lead to dehydration, impaired thermoregulation, and energy loss to wound healing. The presence, number and total area of gull-inflicted lesions were assessed using aerial survey photographs of living mother-calf pairs in 1974-2011 (n = 2680) and stranding photographs of dead calves (n = 192) in 2003-2011. The percentage of living mothers and calves with gull lesions increased from an average of 2% in the 1970s to 99% in the 2000s. In the 1980s and 1990s, mothers and calves had roughly equal numbers of lesions (one to five), but by the 2000s, calves had more lesions (nine or more) covering a greater area of their backs compared to their mothers. Living mother-calf pairs and dead calves in Golfo Nuevo had more lesions than those in Golfo San José in the 2000s. The number and area of lesions increased with calf age during the calving season. Intensified Kelp Gull harassment at Península Valdés could be compromising calf health and thereby contributing to the high average rate of calf mortality observed in recent years, but it cannot explain the large year-to-year variance in calf deaths since 2000.

Pacific Ocean-wide profile of CYP1A1 expression, stable carbon and nitrogen isotope ratios, and organic contaminant burden in sperm whale skin biopsies.

BACKGROUND: Ocean pollution affects marine organisms and ecosystems as well as humans. The International Oceanographic Commission recommends ocean health monitoring programs to investigate the presence of marine contaminants and the health of threatened species and the use of multiple and early-warning biomarker approaches. OBJECTIVE: We explored the hypothesis that biomarker and contaminant analyses in skin biopsies of the threatened sperm whale (Physeter macrocephalus) could reveal geographical trends in exposure on an oceanwide scale. METHODS: We analyzed cytochrome P450 1A1 (CYP1A1) expression (by immunohistochemistry), stable nitrogen and carbon isotope ratios (as general indicators of trophic position and latitude, respectively), and contaminant burdens in skin biopsies to explore regional trends in the Pacific Ocean. RESULTS: Biomarker analyses revealed significant regional differences within the Pacific Ocean. CYP1A1 expression was highest in whales from the Galapagos, a United Nations Educational, Scientific, and Cultural Organization World Heritage marine reserve, and was lowest in the sampling sites farthest away from continents. We examined the possible influence of the whales' sex, diet, or range and other parameters on regional variation in CYP1A1 expression, but data were inconclusive. In general, CYP1A1 expression was not significantly correlated with contaminant burdens in blubber. However, small sample sizes precluded detailed chemical analyses, and power to detect significant associations was limited. CONCLUSIONS: Our large-scale monitoring study was successful at identifying regional differences in CYP1A1 expression, providing a baseline for this known biomarker of exposure to aryl hydrocarbon receptor agonists. However, we could not identify factors that explained this variation. Future oceanwide CYP1A1 expression profiles in cetacean skin biopsies are warranted and could reveal whether globally distributed chemicals occur at biochemically relevant concentrations on a global basis, which may provide a measure of ocean integrity.

Gene genealogies strongly distorted by weakly interfering mutations in constant environments.

Neutral nucleotide diversity does not scale with population size as expected, and this "paradox of variation" is especially severe for animal mitochondria. Adaptive selective sweeps are often proposed as a major cause, but a plausible alternative is selection against large numbers of weakly deleterious mutations subject to Hill-Robertson interference. The mitochondrial genealogies of several species of whale lice (Amphipoda: Cyamus) are consistently too short relative to neutral-theory expectations, and they are also distorted in shape (branch-length proportions) and topology (relative sister-clade sizes). This pattern is not easily explained by adaptive sweeps or demographic history, but it can be reproduced in models of interference among forward and back mutations at large numbers of sites on a nonrecombining chromosome. A coalescent simulation algorithm was used to study this model over a wide range of parameter values. The genealogical distortions are all maximized when the selection coefficients are of critical intermediate sizes, such that Muller's ratchet begins to turn. In this regime, linked neutral nucleotide diversity becomes nearly insensitive to N. Mutations of this size dominate the dynamics even if there are also large numbers of more strongly and more weakly selected sites in the genome. A genealogical perspective on Hill-Robertson interference leads directly to a generalized background-selection model in which the effective population size is progressively reduced going back in time from the present.

Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis).

Ocean warming will undoubtedly affect the migratory patterns of many marine species, but specific changes can be predicted only where behavioural mechanisms guiding migration are understood. Southern right whales show maternally inherited site fidelity to near-shore winter nursery grounds, but exactly where they feed in summer (collectively and individually) remains mysterious. They consume huge quantities of copepods and krill, and their reproductive rates respond to fluctuations in krill abundance linked to El Niño Southern Oscillation (ENSO). Here we show that genetic and isotopic signatures, analysed together, indicate maternally directed site fidelity to diverse summer feeding grounds for female right whales calving at Península Valdés, Argentina. Isotopic values from 131 skin samples span a broad range (-23.1 to -17.2‰ δ¹³C, 6.0 to 13.8‰ δ¹5N) and are more similar than expected among individuals sharing the same mitochondrial haplotype. This pattern indicates that calves learn summer feeding locations from their mothers, and that the timescale of culturally inherited site fidelity to feeding grounds is at least several generations. Such conservatism would be expected to limit the exploration of new feeding opportunities, and may explain why this population shows increased rates of reproductive failure in years following elevated sea-surface temperature anomalies off South Georgia, the richest known feeding ground for baleen whales in the South Atlantic.

Global climate drives southern right whale (Eubalaena australis) population dynamics.

Sea surface temperature (SST) time-series from the southwest Atlantic and the El Niño 4 region in the western Pacific were compared to an index of annual calving success of the southern right whale (Eubalaena australis) breeding in Argentina. There was a strong relationship between right whale calving output and SST anomalies at South Georgia in the autumn of the previous year and also with mean El Niño 4 SST anomalies delayed by 6 years. These results extend similar observations from other krill predators and show clear linkages between global climate signals and the biological processes affecting whale population dynamics.

Population histories of right whales (Cetacea: Eubalaena) inferred from mitochondrial sequence diversities and divergences of their whale lice (Amphipoda: Cyamus).

Right whales carry large populations of three 'whale lice' (Cyamus ovalis, Cyamus gracilis, Cyamus erraticus) that have no other hosts. We used sequence variation in the mitochondrial COI gene to ask (i) whether cyamid population structures might reveal associations among right whale individuals and subpopulations, (ii) whether the divergences of the three nominally conspecific cyamid species on North Atlantic, North Pacific, and southern right whales (Eubalaena glacialis, Eubalaena japonica, Eubalaena australis) might indicate their times of separation, and (iii) whether the shapes of cyamid gene trees might contain information about changes in the population sizes of right whales. We found high levels of nucleotide diversity but almost no population structure within oceans, indicating large effective population sizes and high rates of transfer between whales and subpopulations. North Atlantic and Southern Ocean populations of all three species are reciprocally monophyletic, and North Pacific C. erraticus is well separated from North Atlantic and southern C. erraticus. Mitochondrial clock calibrations suggest that these divergences occurred around 6 million years ago (Ma), and that the Eubalaena mitochondrial clock is very slow. North Pacific C. ovalis forms a clade inside the southern C. ovalis gene tree, implying that at least one right whale has crossed the equator in the Pacific Ocean within the last 1-2 million years (Myr). Low-frequency polymorphisms are more common than expected under neutrality for populations of constant size, but there is no obvious signal of rapid, interspecifically congruent expansion of the kind that would be expected if North Atlantic or southern right whales had experienced a prolonged population bottleneck within the last 0.5 Myr.