Whiskers provide time-series of toxic and essential trace elements, Se:Hg molar ratios, and stable isotope values of an apex Antarctic predator, the leopard seal.

In an era of rapid environmental change and increasing human presence, researchers need efficient tools for tracking contaminants to monitor the health of Antarctic flora and fauna. Here, we examined the utility of leopard seal whiskers as a biomonitoring tool that reconstructs time-series of significant ecological and physiological biomarkers. Leopard seals (Hydrurga leptonyx) are a sentinel species in the Western Antarctic Peninsula due to their apex predator status and top-down effects on several Antarctic species. However, there are few data on their contaminant loads. We analyzed leopard seal whiskers (n = 18 individuals, n = 981 segments) collected during 2018-2019 field seasons to acquire longitudinal profiles of non-essential (Hg, Pb, and Cd) and essential (Se, Cu, and Zn) trace elements, stable isotope (ẟ15N and ẟ13C) values and to assess Hg risk with Se:Hg molar ratios. Whiskers provided between 46 and 286 cumulative days of growth with a mean ~ 125 days per whisker (n = 18). Adult whiskers showed variability in non-essential trace elements over time that could partly be explained by changes in diet. Whisker Hg levels were insufficient (<20 ppm) to consider most seals being at "high" risk for Hg toxicity. Nevertheless, maximum Hg concentrations observed in this study were greater than that of leopard seal hair measured two decades ago. However, variation in the Se:Hg molar ratios over time suggest that Se may detoxify Hg burden in leopard seals. Overall, we provide evidence that the analysis of leopard seal whiskers allows for the reconstruction of time-series ecological and physiological data and can be valuable for opportunistically monitoring the health of the leopard seal population and their Antarctic ecosystem during climate change.

Evolution: Killer whale bites and appetites.

A newly discovered fossil dolphin shows that modern killer and false-killer whales evolved from fish-eating ancestors. While today both species occasionally feed on large warm-blooded prey, including seals and other whales, this diet specialization has evolved only recently.

Trade-offs between foraging reward and mortality risk drive sex-specific foraging strategies in sexually dimorphic northern elephant seals.

Sex-specific phenotypic differences are widespread throughout the animal kingdom. Reproductive advantages provided by trait differences come at a cost. Here, we link sex-specific foraging strategies to trade-offs between foraging reward and mortality risk in sexually dimorphic northern elephant seals (Mirounga angustirostris). We analyse a decadal dataset on movement patterns, dive behaviour, foraging success and mortality rates. Females are deep-diving predators in open ocean habitats. Males are shallow-diving benthic predators in continental shelf habitats. Males gain six times more mass and acquire energy 4.1 times faster than females. High foraging success comes with a high mortality rate. Males are six times more likely to die than females. These foraging strategies and trade-offs are related to different energy demands and life-history strategies. Males use a foraging strategy with a high mortality risk to attain large body sizes necessary to compete for females, as only a fraction of the largest males ever mate. Females use a foraging strategy with a lower mortality risk, maximizing reproductive success by pupping annually over a long lifespan. Our results highlight how sex-specific traits can drive disparity in mortality rates and expand species' niche space. Further, trade-offs between foraging rewards and mortality risk can differentially affect each sex's ability to maximize fitness.

Comparative examination of pinniped craniofacial musculature and its role in aquatic feeding.

Secondarily aquatic tetrapods have many unique morphologic adaptations for life underwater compared with their terrestrial counterparts. A key innovation during the land-to-water transition was feeding. Pinnipeds, a clade of air-breathing marine carnivorans that include seals, sea lions, and walruses, have evolved multiple strategies for aquatic feeding (e.g., biting, suction feeding). Numerous studies have examined the pinniped skull and dental specializations for underwater feeding. However, data on the pinniped craniofacial musculoskeletal system and its role in aquatic feeding are rare. Therefore, the objectives of this study were to conduct a comparative analysis of pinniped craniofacial musculature and examine the function of the craniofacial musculature in facilitating different aquatic feeding strategies. We performed anatomic dissections of 35 specimens across six pinniped species. We describe 32 pinniped craniofacial muscles-including facial expression, mastication, tongue, hyoid, and soft palate muscles. Pinnipeds broadly conform to mammalian patterns of craniofacial muscle morphology. Pinnipeds also exhibit unique musculoskeletal morphologies-in muscle position, attachments, and size-that likely represent adaptations for different aquatic feeding strategies. Suction feeding specialists (bearded and northern elephant seals) have a significantly larger masseter than biters. Further, northern elephant seals have large and unique tongue and hyoid muscle morphologies compared with other pinniped species. These morphologic changes likely help generate and withstand suction pressures necessary for drawing water and prey into the mouth. In contrast, biting taxa (California sea lions, harbor, ringed, and Weddell seals) do not exhibit consistent craniofacial musculoskeletal adaptations that differentiate them from suction feeders. Generally, we discover that all pinnipeds have well-developed and robust craniofacial musculature. Pinniped head musculature plays an important role in facilitating different aquatic feeding strategies. Together with behavioral and kinematic studies, our data suggest that pinnipeds' robust facial morphology allows animals to switch feeding strategies depending on the environmental context-a critical skill in a heterogeneous and rapidly changing underwater habitat.

A continuous-time state-space model for rapid quality control of argos locations from animal-borne tags.

BACKGROUND: State-space models are important tools for quality control and analysis of error-prone animal movement data. The near real-time (within 24 h) capability of the Argos satellite system can aid dynamic ocean management of human activities by informing when animals enter wind farms, shipping lanes, and other intensive use zones. This capability also facilitates the use of ocean observations from animal-borne sensors in operational ocean forecasting models. Such near real-time data provision requires rapid, reliable quality control to deal with error-prone Argos locations. METHODS: We formulate a continuous-time state-space model to filter the three types of Argos location data (Least-Squares, Kalman filter, and Kalman smoother), accounting for irregular timing of observations. Our model is deliberately simple to ensure speed and reliability for automated, near real-time quality control of Argos location data. We validate the model by fitting to Argos locations collected from 61 individuals across 7 marine vertebrates and compare model-estimated locations to contemporaneous GPS locations. We then test assumptions that Argos Kalman filter/smoother error ellipses are unbiased, and that Argos Kalman smoother location accuracy cannot be improved by subsequent state-space modelling. RESULTS: Estimation accuracy varied among species with Root Mean Squared Errors usually <5 km and these decreased with increasing data sampling rate and precision of Argos locations. Including a model parameter to inflate Argos error ellipse sizes in the north - south direction resulted in more accurate location estimates. Finally, in some cases the model appreciably improved the accuracy of the Argos Kalman smoother locations, which should not be possible if the smoother is using all available information. CONCLUSIONS: Our model provides quality-controlled locations from Argos Least-Squares or Kalman filter data with accuracy similar to or marginally better than Argos Kalman smoother data that are only available via fee-based reprocessing. Simplicity and ease of use make the model suitable both for automated quality control of near real-time Argos data and for manual use by researchers working with historical Argos data.

Context Matters: Hawaiian Monk Seals Switch Between Feeding Strategies Depending on Ecological Context.

The ability to expand the behavioral repertoire past seemingly rigid morphological features enables animals to succeed in a variety of ecological contexts. The integration of morphology, performance, and behavior produces diverse animal feeding strategies. These different strategies reflect trade-offs between specialization, prey choice, and energetic expenditure, which have important consequences for understanding individual and population-level flexibility in response to environmental change. Here we examined the feeding strategies used by the Hawaiian monk seal (Neomonachus schauinslandi), an endangered marine predator. We tested how Hawaiian monk seal feeding strategies change in response to ecological context, specifically prey size and prey location at different depths. Seven captive Hawaiian monk seals were fed five prey types across a continuum of sizes, and prey were presented at three depths to represent surface, pelagic, and benthic feeding. Hawaiian monk seals used suction feeding and biting strategies, and these strategies were associated with significant differences in behavior and kinematic performance. Hawaiian monk seals used suction feeding most frequently when targeting small to medium prey (0-79% of the seal's head length) but switched to biting when consuming large prey (>80% of the seal's head length). These results demonstrate that prey size drives the transition between suction feeding and biting strategies. Seals also switched strategies based on prey position in the water column, primarily using suction feeding when prey were benthic and pelagic, and biting when prey were at the water's surface. Overall, suction feeding was three to five times faster than biting, required a smaller gape, and used fewer jaw movements, allowing seals to quickly consume numerous small to medium sized prey. In contrast, biting was slower but resulted in the ability to target larger, potentially more energy rich prey. Our results show that Hawaiian monk seals exhibit flexibility in their use of different feeding strategies, which likely facilitates increased foraging success when feeding in spatially and temporally dynamic marine environments.

Hawaiian monk seals exhibit behavioral flexibility when targeting prey of different size and shape.

Animals use diverse feeding strategies to capture and consume prey, with many species switching between strategies to accommodate different prey. Many marine animals exhibit behavioral flexibility when feeding to deal with spatial and temporal heterogeneity in prey resources. However, little is known about flexibility in the feeding behavior of many large marine predators. Here, we documented the feeding behavior and kinematics of the endangered Hawaiian monk seal (Neomonachus schauinslandi, n=7) through controlled feeding trials. Seals were fed multiple prey types (e.g. night smelt, capelin, squid and herring) that varied in size and shape to examine behavioral flexibility in feeding. Hawaiian monk seals primarily used suction feeding (91% of all feeding trials) across all prey types, but biting, specifically pierce feeding, was also observed (9% of all feeding trials). Suction feeding was characterized by shorter temporal events, a smaller maximum gape and gape angle, and a fewer number of jaw motions than pierce feeding; suction feeding kinematic performance was also more variable compared with pierce feeding. Seals showed behavioral flexibility in their use of the two strategies. Suction feeding was used most frequently when targeting small to medium sized prey and biting was used with increasing frequency on larger prey. The feeding kinematics differed between feeding strategies and prey types, showing that Hawaiian monk seals adjusted their behaviors to particular feeding contexts. Hawaiian monk seals are opportunistic marine predators and their ability to adapt their feeding strategy and behavior to specific foraging scenarios allows them to target diverse prey resources.

Comparative feeding strategies and kinematics in phocid seals: suction without specialized skull morphology.

Feeding kinematic studies inform our understanding of behavioral diversity and provide a framework for studying the flexibility and constraints of different prey acquisition strategies. However, little is known about the feeding behaviors used by many marine mammals. We characterized the feeding behaviors and associated kinematics of captive bearded (Erignathus barbatus), harbor (Phoca vitulina), ringed (Pusa hispida) and spotted (Phoca largha) seals through controlled feeding trials. All species primarily used a suction feeding strategy but were also observed using a biting strategy, specifically pierce feeding. Suction feeding was distinct from pierce feeding and was characterized by significantly faster feeding times, smaller gapes and gape angles, smaller gular depressions and fewer jaw motions. Most species showed higher variability in suction feeding performance than in pierce feeding, indicating that suction feeding is a behaviorally flexible strategy. Bearded seals were the only species for which there was strong correspondence between skull and dental morphology and feeding strategy, providing further support for their classification as suction feeding specialists. Harbor, ringed and spotted seals have been classified as pierce feeders based on skull and dental morphologies. Our behavioral and kinematic analyses show that suction feeding is also an important feeding strategy for these species, indicating that skull morphology alone does not capture the true diversity of feeding behaviors used by pinnipeds. The ability of all four species to use more than one feeding strategy is likely advantageous for foraging in spatially and temporally dynamic marine ecosystems that favor opportunistic predators.

The better to eat you with: the comparative feeding morphology of phocid seals (Pinnipedia, Phocidae).

One adaptation crucial to the survival of mammalian lineages that secondarily transitioned from land to water environments was the ability to capture and consume prey underwater. Phocid seals have evolved diverse feeding strategies to feed in the marine environment, and the objectives of this study were to document the specialized feeding morphologies and identify feeding strategies used by extant phocids. This study used principal component analysis (PCA) to determine the major axes of diversification in the skull for all extant phocid taxa and the recently extinct Caribbean monk seal (n = 19). Prey data gathered from the literature and musculoskeletal data from dissections were included to provide a comprehensive description of each feeding strategy. Random Forest analysis was used to determine the morphological, ecological and phylogenetic variables that best described each feeding strategy. There is morphological evidence for four feeding strategies in phocids: filter; grip and tear; suction; and pierce feeding. These feeding strategies are supported by quantitative cranial and mandibular characters, dietary information, musculoskeletal data and, for some species, behavioral observations. Most phocid species are pierce feeders, using a combination of biting and suction to opportunistically catch prey. Grip and tear and filter feeding are specialized strategies with specific morphological adaptations. These unique adaptations have allowed leopard seals (Hydrurga leptonyx) and crabeater seals (Lobodon carcinophaga) to exploit novel ecological niches and prey types. This study provides the first cranial and mandibular morphological evidence for the use of specialized suction feeding in hooded seals (Cystophora cristata), northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The most important variables in determining the feeding strategy of a given phocid species were cranial and mandibular shape, diet, and phylogeny. These results provide a framework for understanding the evolution and adaptability of feeding strategies employed by extant phocid species, and these findings can be applied to other pinniped lineages and extinct taxa.

Passive restriction of blood flow and counter-current heat exchange via lingual retia in the tongue of a neonatal gray whale Eschrichtius robustus (Cetacea, Mysticeti).

Retia mirabilia play broad roles in cetacean physiology, including thermoregulation during feeding and pressure regulations during diving. Vascular bundles of lingual retia are described within the base of the tongue of a neonatal female gray whale (Eschrichtius robustus). Each rete consists of a central artery surrounded by four to six smaller veins. The retia and constituent vessels decrease in diameter as they extend anteriorly within the hyoglossus muscle from a position anterior to the basihyal cartilage toward the apex of the tongue. The position of the retia embedded in the hyoglossus and the anterior constriction of the vessels differs from reports of similar vascular bundles that were previously identified in gray whales. The retia likely serve as a counter-current heat exchange system to control body temperature during feeding. Cold blood flowing toward the body center within the periarterial veins would accept heat from warm blood in the central artery flowing toward the anterior end of the tongue. Although thermoregulatory systems have been identified within the mouths of a few mysticete species, the distribution of such vascular structures likely is more widespread among baleen whales than has previously been described.

Eye, nose, hair, and throat: external anatomy of the head of a neonate gray whale (Cetacea, Mysticeti, Eschrichtiidae).

Information is scarce on gray whale (Eschrichtius robustus) anatomy and that of mysticetes in general. Dissection of the head of a neonatal gray whale revealed novel anatomical details of the eye, blowhole, incisive papilla with associated nasopalatine ducts, sensory hairs, and throat grooves. Compared to a similar sized right whale calf, the gray whale eyeball is nearly twice as long. The nasal cartilages of the gray whale, located between the blowholes, differ from the bowhead in having accessory cartilages. A small, fleshy incisive papilla bordered by two blind nasopalatine pits near the palate's rostral tip, previously undescribed in gray whales, may be associated with the vomeronasal organ, although histological evidence is needed for definitive identification. Less well known among mysticetes are the numerous elongated, stiff sensory hairs (vibrissae) observed on the gray whale rostrum from the ventral tip to the blowhole and on the mandible. These hairs are concentrated on the chin, and those on the lower jaw are arranged in a V-shaped pattern. We confirm the presence of two primary, anteriorly converging throat grooves, confined to the throat region similar to those of ziphiid and physeteroid odontocetes. A third, shorter groove occurs lateral to the left primary groove. The throat grooves in the gray whale have been implicated in gular expansion during suction feeding.

Tongue and hyoid musculature and functional morphology of a neonate gray whale (Cetacea, Mysticeti, Eschrichtius robustus).

Little is known about the anatomy and musculature of the gray whale (Eschrichtius robustus), especially related to the anatomy of the tongue and hyoid region. The recovery of an extremely fresh head of a neonatal female gray whale provided an opportunity to conduct the first in-depth investigation of the musculoskeletal features of the tongue and hyoid apparatus. Unlike other mysticetes, the gray whale tongue is strong, muscular, and freely mobile inside the buccal cavity. In particular, the genioglossus and hyoglossus muscles are extremely large and robust making up the majority of the body of the tongue. In addition, the genioglossus had a unique position and fiber orientation in the tongue compared to other mammals. The structure of the hyoid apparatus differs between E. robustus and other mysticete species, although there are similarities among individual elements. We provide the first documentation of fungiform papillae that may be associated with taste buds in Mysticeti. The highly mobile, robust tongue and the presence of well-defined tongue and hyoid musculature are in keeping with observations of gray whale feeding that suggest this group of whales utilize oral suction to draw benthic prey into the buccal cavity.