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.

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.

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.

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.

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.