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.

Mechanisms of auditory masking in marine mammals.

Anthropogenic noise is an increasing threat to marine mammals that rely on sound for communication, navigation, detecting prey and predators, and finding mates. Auditory masking is one consequence of anthropogenic noise, the study of which is approached from multiple disciplines including field investigations of animal behavior, noise characterization from in-situ recordings, computational modeling of communication space, and hearing experiments conducted in the laboratory. This paper focuses on laboratory hearing experiments applying psychophysical methods, with an emphasis on the mechanisms that govern auditory masking. Topics include tone detection in simple, complex, and natural noise; mechanisms for comodulation masking release and other forms of release from masking; the role of temporal resolution in auditory masking; and energetic vs informational masking.

Tracking arctic marine mammal resilience in an era of rapid ecosystem alteration.

Global warming is significantly altering arctic marine ecosystems. Specifically, the precipitous loss of sea ice is creating a dichotomy between ice-dependent polar bears and pinnipeds that are losing habitat and some cetaceans that are gaining habitat. While final outcomes are hard to predict for the many and varied marine mammal populations that rely on arctic habitats, we suggest a simplified framework to assess status, based upon ranking a population's size, range, behavior, and health. This basic approach is proposed as a means to prioritize and expedite conservation and management efforts in an era of rapid ecosystem alteration.

Drivers of the dive response in pinnipeds; apnea, submergence or temperature?

Long and deep dives in marine mammals are enabled by high mass-specific oxygen stores and the dive response, which reduces oxygen consumption in concert with increased peripheral vasoconstriction and a lowered heart rate during dives. Diving heart rates of pinnipeds are highly variable and modulated by many factors, such as breath holding (apnea), pressure, swimming activity, temperature and even cognitive control. However, the individual effects of these factors on diving heart rate are poorly understood because of the difficulty of parsing their relative contributions in diving pinnipeds. Here, we examined the effects of apnea and external sensory inputs as autonomic drivers of bradycardia. Specifically, we hypothesized that (1) water stimulation of facial receptors would - as is the case for terrestrial mammals - enhance the dive response, (2) increasing the facial area stimulated would lead to a more intense bradycardia, and (3) cold water would elicit a more pronounced bradycardia than warm water. Three harbor seals (Phoca vitulina) and a California sea lion (Zalophus californianus) were trained to breath hold in air and with their heads submerged in a basin with variable water level and temperature. We show that bradycardia occurs during apnea without immersion. We also demonstrate that bradycardia is strengthened by both increasing the area of facial submersion and colder water. Thus, we conclude that the initiation of the dive response in pinnipeds is more strongly related to breath holding than in terrestrial mammals, but the degree of the dive response is potentiated autonomically via stimulation of facial mechano- and thermo-receptors upon submergence.

The caval sphincter in cetaceans and its predicted role in controlling venous flow during a dive.

A sphincter on the inferior vena cava can protect the heart of a diving mammal from overload when elevated abdominal pressures increase venous return, yet sphincters are reported incompetent or absent in some cetacean species. We previously hypothesized that abdominal pressures are elevated and pulsatile in fluking cetaceans, and that collagen is deposited on the diaphragm according to pressure levels to resist deformation. Here, we tested the hypothesis that cetaceans generating high abdominal pressures need a more robust sphincter than those generating low pressures. We examined diaphragm morphology in seven cetacean and five pinniped species. All odontocetes had morphologically similar sphincters despite large differences in collagen content, and mysticetes had muscle that could modulate caval flow. These findings do not support the hypothesis that sphincter structure correlates with abdominal pressures. To understand why a sphincter is needed, we simulated the impact of oscillating abdominal pressures on caval flow. Under low abdominal pressures, simulated flow oscillated with each downstroke. Under elevated pressures, a vascular waterfall formed, greatly smoothing flow. We hypothesize that cetaceans maintain high abdominal pressures to moderate venous return and protect the heart while fluking, and use their sphincters only during low-fluking periods when abdominal pressures are low. We suggest that pinnipeds, which do not fluke, maintain low abdominal pressures. Simulations also showed that retrograde oscillations could be transmitted upstream from the cetacean abdomen and into the extradural veins, with potentially adverse repercussions for the cerebral circulation. We propose that locomotion-generated pressures have influenced multiple aspects of the cetacean vascular system.

A behavioural framework for the evolution of feeding in predatory aquatic mammals.

Extant aquatic mammals are a key component of aquatic ecosystems. Their morphology, ecological role and behaviour are, to a large extent, shaped by their feeding ecology. Nevertheless, the nature of this crucial aspect of their biology is often oversimplified and, consequently, misinterpreted. Here, we introduce a new framework that categorizes the feeding cycle of predatory aquatic mammals into four distinct functional stages (prey capture, manipulation and processing, water removal and swallowing), and details the feeding behaviours that can be employed at each stage. Based on this comprehensive scheme, we propose that the feeding strategies of living aquatic mammals form an evolutionary sequence that recalls the land-to-water transition of their ancestors. Our new conception helps to explain and predict the origin of particular feeding styles, such as baleen-assisted filter feeding in whales and raptorial 'pierce' feeding in pinnipeds, and informs the structure of present and past ecosystems.

Controlling thoracic pressures in cetaceans during a breath-hold dive: importance of the diaphragm.

Internal pressures change throughout a cetacean's body during swimming or diving, and uneven pressures between the thoracic and abdominal compartments can affect the cardiovascular system. Pressure differentials could arise from ventral compression on each fluke downstroke or by a faster equilibration of the abdominal compartment with changing ambient ocean pressures compared with the thoracic compartment. If significant pressure differentials do develop, we would expect the morphology of the diaphragm to adapt to its in vivo loading. Here, we tested the hypothesis that significant pressure differentials develop between the thoracic and abdominal cavities in diving cetaceans by examining diaphragms from several cetacean and pinniped species. We found that: (1) regions of cetacean diaphragms possess subserosal collagen fibres that would stabilize the diaphragm against craniocaudal stretch; (2) subserosal collagen covers 5-60% of the thoracic diaphragm surface, and area correlates strongly with published values for swimming speed of each cetacean species (P<0.001); and (3) pinnipeds, which do not locomote by vertical fluking, do not possess this subserosal collagen. These results strongly suggest that this collagen is associated with loads experienced during a dive, and they support the hypothesis that diving cetaceans experience periods during which abdominal pressures significantly exceed thoracic pressures. Our results are consistent with the generation of pressure differentials by fluking and by different compartmental equilibration rates. Pressure differentials during diving would affect venous and arterial perfusion and alter transmural pressures in abdominal arteries.

Respiratory function and mechanics in pinnipeds and cetaceans.

In this Review, we focus on the functional properties of the respiratory system of pinnipeds and cetaceans, and briefly summarize the underlying anatomy; in doing so, we provide an overview of what is currently known about their respiratory physiology and mechanics. While exposure to high pressure is a common challenge among breath-hold divers, there is a large variation in respiratory anatomy, function and capacity between species - how are these traits adapted to allow the animals to withstand the physiological challenges faced during dives? The ultra-deep diving feats of some marine mammals defy our current understanding of respiratory physiology and lung mechanics. These animals cope daily with lung compression, alveolar collapse, transient hyperoxia and extreme hypoxia. By improving our understanding of respiratory physiology under these conditions, we will be better able to define the physiological constraints imposed on these animals, and how these limitations may affect the survival of marine mammals in a changing environment. Many of the respiratory traits to survive exposure to an extreme environment may inspire novel treatments for a variety of respiratory problems in humans.

A comparison of blood nitric oxide metabolites and hemoglobin functional properties among diving mammals.

The ability of marine mammals to hunt prey at depth is known to rely on enhanced oxygen stores and on selective distribution of blood flow, but the molecular mechanisms regulating blood flow and oxygen transport remain unresolved. To investigate the molecular mechanisms that may be important in regulating blood flow, we measured concentration of nitrite and S-nitrosothiols (SNO), two metabolites of the vasodilator nitric oxide (NO), in the blood of 5 species of marine mammals differing in their dive duration: bottlenose dolphin, South American sea lion, harbor seal, walrus and beluga whale. We also examined oxygen affinity, sensitivity to 2,3-diphosphoglycerate (DPG) and nitrite reductase activity of the hemoglobin (Hb) to search for possible adaptive variations in these functional properties. We found levels of plasma and red blood cells nitrite similar to those reported for terrestrial mammals, but unusually high concentrations of red blood cell SNO in bottlenose dolphin, walrus and beluga whale, suggesting enhanced SNO-dependent signaling in these species. Purified Hbs showed similar functional properties in terms of oxygen affinity and sensitivity to DPG, indicating that reported large variations in blood oxygen affinity among diving mammals likely derive from phenotypic variations in red blood cell DPG levels. The nitrite reductase activities of the Hbs were overall slightly higher than that of human Hb, with the Hb of beluga whale, capable of longest dives, having the highest activity. Taken together, these results underscore adaptive variations in circulatory NO metabolism in diving mammals but not in the oxygenation properties of the Hb.

Contrasting responses to a climate regime change by sympatric, ice-dependent predators.

BACKGROUND: Models that predict changes in the abundance and distribution of fauna under future climate change scenarios often assume that ecological niche and habitat availability are the major determinants of species' responses to climate change. However, individual species may have very different capacities to adapt to environmental change, as determined by intrinsic factors such as their dispersal ability, genetic diversity, generation time and rate of evolution. These intrinsic factors are usually excluded from forecasts of species' abundance and distribution changes. We aimed to determine the importance of these factors by comparing the impact of the most recent climate regime change, the late Pleistocene glacial-interglacial transition, on two sympatric, ice-dependent meso-predators, the emperor penguin (Aptenodytes forsteri) and Weddell seal (Leptonychotes weddellii). METHODS: We reconstructed the population trend of emperor penguins and Weddell seals in East Antarctica over the past 75,000 years using mitochondrial DNA sequences and an extended Bayesian skyline plot method. We also assessed patterns of contemporary population structure and genetic diversity. RESULTS: Despite their overlapping distributions and shared dependence on sea ice, our genetic data revealed very different responses to climate warming between these species. The emperor penguin population grew rapidly following the glacial-interglacial transition, but the size of the Weddell seal population did not change. The expansion of emperor penguin numbers during the warm Holocene may have been facilitated by their higher dispersal ability and gene flow among colonies, and fine-scale differences in preferred foraging locations. CONCLUSIONS: The vastly different climate change responses of two sympatric ice-dependent predators suggests that differing adaptive capacities and/or fine-scale niche differences can play a major role in species' climate change responses, and that adaptive capacity should be considered alongside niche and distribution in future species forecasts.

The evolution of aquatic feeding in seals: insights from Enaliarctos (Carnivora: Pinnipedimorpha), the oldest known seal.

The development of pierce-feeding and loss of oral processing represented major adaptations for underwater feeding in marine mammals. We examined the evolution of pierce-feeding and its association with changes in tooth spacing and tooth size to determine whether pierce-feeding was practiced by the earliest known pinnipeds. Data on crown size and spacing in postcanine dentition were collected and 1) analysed by principal components analysis (PCA) to determine the tooth morphospace of arctoid carnivores, 2) analysed by least squares (LS) regression and phylogenetic independent contrasts (PIC) to determine what morphological variables were associated with increases in tooth spacing, and 3) used to reconstruct the evolution of feeding related traits within a phylogenetic context. The PCA analysis revealed that within arctoid carnivores, the greatest differences in morphospace were associated with pierce-feeding, and the early-diverging seal Enaliarctos was placed within the pinniped morphospace. Increased tooth spacing within Pinnipedia is a result of decreased postcanine crown size. When the evolution of dental characters is reconstructed, 'enaliarctines' were found to represent an intermediate stage in evolution between 'fissiped' and pinniped carnivores. They retained the limited tooth spacing of terrestrial carnivores, possessed postcanine crown lengths intermediate in size between pinnipeds and fissipeds, and possessed reduced heterodonty characteristic of crown pinnipeds. Our study indicated that pierce-feeding evolved early within pinnipeds. This suggested either that pierce-feeding evolved prior to the loss of mastication, or that pierce-feeding evolved at the same time as loss of mastication, and well before simplification of the dentition was completed.

Marine Mammals in the Mediterranean Sea: An Overview.

Despite being a small part of the world's oceans, the Mediterranean Sea hosts a diverse marine mammal fauna, with a total of 28 different species known to occur, or to have occurred, in the region. Species currently recognised as regular in the Mediterranean-the Mediterranean monk seal (Monachus monachus) and 11 cetaceans (fin whale, Balaenoptera physalus; sperm whale, Physeter macrocephalus; Cuvier's beaked whale, Ziphius cavirostris; short-beaked common dolphin, Delphinus delphis; long-finned pilot whale, Globicephala melas; Risso's dolphin, Grampus griseus; killer whale, Orcinus orca; striped dolphin, Stenella coeruleoalba; rough-toothed dolphin, Steno bredanensis; common bottlenose dolphin, Tursiops truncatus; harbour porpoise, Phocoena phocoena relicta) have adapted well to the region's environmental conditions, but their coexistence with humans is problematic. All the regular species are represented in the Mediterranean by populations genetically distinct from their North Atlantic relatives. Seventeen other species (three pinnipeds and 14 cetaceans) occur or have occurred in the Mediterranean as vagrants from adjacent regions. Impacts on the conservation status of marine mammals in the region deriving from a variety of threats include: (a) mortality caused by deliberate killing (to a large extent resulting from fisheries interactions), naval sonar, ship strikes, epizootics, fisheries bycatch, chemical pollution and ingestion of solid debris; (b) short-term redistribution caused by naval sonar, seismic surveys, vessel disturbance and vessel noise; and (c) long-term redistribution caused by fishery-induced food depletion, coastal development and possibly climate change. Accordingly, seven of the 12 marine mammals regular in the Mediterranean region are listed as Threatened on IUCN's Red List; regrettably, three are Data Deficient and two remain unassessed.

Psychoacoustic Studies of Spotted (Phoca largha) and Ringed (Pusa hispida) Seals.

Human development of the marine environment raises questions regarding the potential adverse effects of anthropogenic noise on marine mammals. For species that live in remote Arctic regions, recent and expanding human intrusions may pose a particular threat. Northern seals are poorly studied relative to their temperate counterparts and little is known of their acoustic ecology or behavior. Given this scarcity of relevant data, studies of hearing in Arctic seals are essential to characterize their auditory capabilities and to inform management decisions. This paper describes ongoing psychoacoustic studies that are examining aspects of hearing in two ice seal species.

Impacts of Underwater Noise on Marine Vertebrates: Project Introduction and First Results.

The project conducts application-oriented research on impacts of underwater noise on marine vertebrates in the North and Baltic Seas. In distinct subprojects, the hearing sensitivity of harbor porpoises and gray seals as well as the acoustic tolerance limit of harbor porpoises to impulsive noise from pile driving and stress reactions caused by anthropogenic noise is investigated. Animals are equipped with DTAGs capable of recording the actual surrounding noise field of free-swimming harbor porpoises and seals. Acoustic noise mapping including porpoise detectors in the Natura 2000 sites of the North and Baltic Seas will help to fully understand current noise impacts.

Diving physiology of seabirds and marine mammals: Relevance, challenges and some solutions for field studies.

To fully understand how diving seabirds and marine mammals balance the potentially conflicting demands of holding their breath while living their lives underwater (and maintaining physiological homeostasis during exercise, feeding, growth, and reproduction), physiological studies must be conducted with animals in their natural environments. The purpose of this article is to review the importance of making physiological measurements on diving animals in field settings, while acknowledging the challenges and highlighting some solutions. The most extreme divers are great candidates for study, especially in a comparative and mechanistic context. However, physiological data are also required of a wide range of species for problems relating to other disciplines, in particular ecology and conservation biology. Physiological data help with understanding and predicting the outcomes of environmental change, and the direct impacts of anthropogenic activities. Methodological approaches that have facilitated the development of field-based diving physiology include the isolated diving hole protocol and the translocation paradigm, and while there are many techniques for remote observation, animal-borne biotelemetry, or "biologging", has been critical. We discuss issues related to the attachment of instruments, the retrieval of data and sensing of physiological variables, while also considering negative impacts of tagging. This is illustrated with examples from a variety of species, and an in-depth look at one of the best studied and most extreme divers, the emperor penguin (Aptenodytes forsteri). With a variety of approaches and high demand for data on the physiology of diving seabirds and marine mammals, the future of field studies is bright.

Taking animal tracking to new depths: synthesizing horizontal--vertical movement relationships for four marine predators.

In animal ecology, a question of key interest for aquatic species is how changes in movement behavior are related in the horizontal and vertical dimensions when individuals forage. Alternative theoretical models and inconsistent empirical findings mean that this question remains unresolved. Here we tested expectations by incorporating the vertical dimension (dive information) when predicting switching between movement states ("resident" or "directed") within a state-space model. We integrated telemetry-based tracking and diving data available for four seal species (southern elephant, Weddell, antarctic fur, and crabeater) in East Antarctica. Where possible, we included dive variables derived from the relationships between (1) dive duration and depth (as a measure of effort), and (2) dive duration and the postdive surface interval (as a physiological measure of cost). Our results varied within and across species, but there was a general tendency for the probability of switching into "resident" state to be positively associated with shorter dive durations (for a given depth) and longer postdive surface intervals (for a given dive duration). Our results add to a growing body of literature suggesting that simplistic interpretations of optimal foraging theory based only on horizontal movements do not directly translate into the vertical dimension in dynamic marine environments. Analyses that incorporate at least two dimensions can test more sophisticated models of foraging behavior.

Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century.

Arctic marine mammals (AMMs) are icons of climate change, largely because of their close association with sea ice. However, neither a circumpolar assessment of AMM status nor a standardized metric of sea ice habitat change is available. We summarized available data on abundance and trend for each AMM species and recognized subpopulation. We also examined species diversity, the extent of human use, and temporal trends in sea ice habitat for 12 regions of the Arctic by calculating the dates of spring sea ice retreat and fall sea ice advance from satellite data (1979-2013). Estimates of AMM abundance varied greatly in quality, and few studies were long enough for trend analysis. Of the AMM subpopulations, 78% (61 of 78) are legally harvested for subsistence purposes. Changes in sea ice phenology have been profound. In all regions except the Bering Sea, the duration of the summer (i.e., reduced ice) period increased by 5-10 weeks and by >20 weeks in the Barents Sea between 1979 and 2013. In light of generally poor data, the importance of human use, and forecasted environmental changes in the 21st century, we recommend the following for effective AMM conservation: maintain and improve comanagement by local, federal, and international partners; recognize spatial and temporal variability in AMM subpopulation response to climate change; implement monitoring programs with clear goals; mitigate cumulative impacts of increased human activity; and recognize the limits of current protected species legislation.

A semi-aquatic Arctic mammalian carnivore from the Miocene epoch and origin of Pinnipedia.

Modern pinnipeds (seals, sea lions and the walrus) are semi-aquatic, generally marine carnivores the limbs of which have been modified into flippers. Recent phylogenetic studies using morphological and molecular evidence support pinniped monophyly, and suggest a sister relationship with ursoids (for example bears) or musteloids (the clade that includes skunks, badgers, weasels and otters). Although the position of pinnipeds within modern carnivores appears moderately well resolved, fossil evidence of the morphological steps leading from a terrestrial ancestor to the modern marine forms has been weak or contentious. The earliest well-represented fossil pinniped is Enaliarctos, a marine form with flippers, which had appeared on the northwestern shores of North America by the early Miocene epoch. Here we report the discovery of a nearly complete skeleton of a new semi-aquatic carnivore from an early Miocene lake deposit in Nunavut, Canada, that represents a morphological link in early pinniped evolution. The new taxon retains a long tail and the proportions of its fore- and hindlimbs are more similar to those of modern terrestrial carnivores than to modern pinnipeds. Morphological traits indicative of semi-aquatic adaptation include a forelimb with a prominent deltopectoral ridge on the humerus, a posterodorsally expanded scapula, a pelvis with relatively short ilium, a shortened femur and flattened phalanges, suggestive of webbing. The new fossil shows evidence of pinniped affinities and similarities to the early Oligocene Amphicticeps from Asia and the late Oligocene and Miocene Potamotherium from Europe. The discovery suggests that the evolution of pinnipeds included a freshwater transitional phase, and may support the hypothesis that the Arctic was an early centre of pinniped evolution.

Drivers and hotspots of extinction risk in marine mammals.

The world's oceans are undergoing profound changes as a result of human activities. However, the consequences of escalating human impacts on marine mammal biodiversity remain poorly understood. The International Union for the Conservation of Nature (IUCN) identifies 25% of marine mammals as at risk of extinction, but the conservation status of nearly 40% of marine mammals remains unknown due to insufficient data. Predictive models of extinction risk are crucial to informing present and future conservation needs, yet such models have not been developed for marine mammals. In this paper, we: (i) used powerful machine-learning and spatial-modeling approaches to understand the intrinsic and extrinsic drivers of marine mammal extinction risk; (ii) used this information to predict risk across all marine mammals, including IUCN "Data Deficient" species; and (iii) conducted a spatially explicit assessment of these results to understand how risk is distributed across the world's oceans. Rate of offspring production was the most important predictor of risk. Additional predictors included taxonomic group, small geographic range area, and small social group size. Although the interaction of both intrinsic and extrinsic variables was important in predicting risk, overall, intrinsic traits were more important than extrinsic variables. In addition to the 32 species already on the IUCN Red List, our model identified 15 more species, suggesting that 37% of all marine mammals are at risk of extinction. Most at-risk species occur in coastal areas and in productive regions of the high seas. We identify 13 global hotspots of risk and show how they overlap with human impacts and Marine Protected Areas.

Noise-induced hearing loss in marine mammals: A review of temporary threshold shift studies from 1996 to 2015.

One of the most widely recognized effects of intense noise exposure is a noise-induced threshold shift­an elevation of hearing thresholds following cessation of the noise. Over the past twenty years, as concerns over the potential effects of human-generated noise on marine mammals have increased, a number of studies have been conducted to investigate noise-induced threshold shift phenomena in marine mammals. The experiments have focused on measuring temporary threshold shift (TTS)­a noise-induced threshold shift that fully recovers over time­in marine mammals exposed to intense tones, band-limited noise, and underwater impulses with various sound pressure levels, frequencies, durations, and temporal patterns. In this review, the methods employed by the groups conducting marine mammal TTS experiments are described and the relationships between the experimental conditions, the noise exposure parameters, and the observed TTS are summarized. An attempt has been made to synthesize the major findings across experiments to provide the current state of knowledge for the effects of noise on marine mammal hearing.