The impact of the land-to-sea transition on evolutionary integration and modularity of the pinniped backbone.

In this study, we investigate how the terrestrial-aquatic transition influenced patterns of axial integration and modularity in response to the secondary adaptation to a marine lifestyle. We use 3D geometric morphometrics to quantify shape covariation among presacral vertebrae in pinnipeds (Carnivora; Pinnipedia) and to compare with patterns of axial integration and modularity in their close terrestrial relatives. Our results indicate that the vertebral column of pinnipeds has experienced a decrease in the strength of integration among all presacral vertebrae when compared to terrestrial carnivores (=fissipeds). However, separate integration analyses among the speciose Otariidae (i.e., sea lions and fur seals) and Phocidae (i.e., true seals) also suggests the presence of different axial organizations in these two groups of crown pinnipeds. While phocids present a set of integrated "thoracic" vertebrae, the presacral vertebrae of otariids are characterized by the absence of any set of vertebrae with high integration. We hypothesize that these differences could be linked to their specific modes of aquatic locomotion -i.e., pelvic vs pectoral oscillation. Our results provide evidence that the vertebral column of pinnipeds has been reorganized from the pattern observed in fissipeds but is more complex than a simple "homogenization" of the modular pattern of their close terrestrial relatives.

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.

Marine mammal sensory systems: Special issue overview.

Marine mammals are a unique group of organisms that are secondarily adapted to the aquatic environment. Their specific lifestyle requires numerous adaptations of anatomy and physiology in general, and sensory physiology in particular. During the course of evolution, marine mammal senses changed to fit with the specific requirements of underwater sensing, while at the same time retaining aerial sensing to various degrees. In this special issue, state of the art science in the field of marine mammal sensory research is reported for representatives of all marine mammal groups, unfortunately with the exclusion of the polar bear. The articles focus on somatosensation of the glabrous skin of cetaceans and mechanoreception, including haptics, hydrodynamics, and acoustics, to chemoreception. Articles even deal with electroreception, highlighting that the bottlenose dolphin can perceive weak electric stimuli, and vision, indicating that harbor seals are able to derive temporal information from an optical stimulus. Altogether this special issue illustrates the diversity of research in the field regarding sensory systems, species, or experimental approaches. The strength of this special issue lies in the combination of carefully conducted anatomical studies paired with observations and behavioral studies attempting to relate "form" and "function" as well as in the many impulses and future avenues mentioned by numerous contributions.

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.

The isotopic niche of Atlantic, biting marine mammals and its relationship to skull morphology and body size.

Understanding the trophic niches of marine apex predators is necessary to understand interactions between species and to achieve sustainable, ecosystem-based fisheries management. Here, we review the stable carbon and nitrogen isotope ratios for biting marine mammals inhabiting the Atlantic Ocean to test the hypothesis that the relative position of each species within the isospace is rather invariant and that common and predictable patterns of resource partitioning exists because of constrains imposed by body size and skull morphology. Furthermore, we analyze in detail two species-rich communities to test the hypotheses that marine mammals are gape limited and that trophic position increases with gape size. The isotopic niches of species were highly consistent across regions and the topology of the community within the isospace was well conserved across the Atlantic Ocean. Furthermore, pinnipeds exhibited a much lower diversity of isotopic niches than odontocetes. Results also revealed body size as a poor predictor of the isotopic niche, a modest role of skull morphology in determining it, no evidence of gape limitation and little overlap in the isotopic niche of sympatric species. The overall evidence suggests limited trophic flexibility for most species and low ecological redundancy, which should be considered for ecosystem-based fisheries management.

An engineering perspective on the development and evolution of implantable cardiac monitors in free-living animals.

The latest technologies associated with implantable physiological monitoring devices can record multiple channels of data (including: heart rates and rhythms, activity, temperature, impedance and posture), and coupled with powerful software applications, have provided novel insights into the physiology of animals in the wild. This perspective details past challenges and lessons learned from the uses and developments of implanted biologgers designed for human clinical application in our research on free-ranging American black bears (Ursus americanus). In addition, we reference other research by colleagues and collaborators who have leveraged these devices in their work, including: brown bears (Ursus arctos), grey wolves (Canis lupus), moose (Alces alces), maned wolves (Chrysocyon brachyurus) and southern elephant seals (Mirounga leonina). We also discuss the potentials for applications of such devices across a range of other species. To date, the devices described have been used in fifteen different wild species, with publications pending in many instances. We have focused our physiological research on the analyses of heart rates and rhythms and thus special attention will be paid to this topic. We then discuss some major expected step changes such as improvements in sensing algorithms, data storage, and the incorporation of next-generation short-range wireless telemetry. The latter provides new avenues for data transfer, and when combined with cloud-based computing, it not only provides means for big data storage but also the ability to readily leverage high-performance computing platforms using artificial intelligence and machine learning algorithms. These advances will dramatically increase both data quantity and quality and will facilitate the development of automated recognition of extreme physiological events or key behaviours of interest in a broad array of environments, thus further aiding wildlife monitoring and management. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

The northernmost haulout site of South American sea lions and fur seals in the western South Atlantic.

We present estimates of the seasonal and spatial occupation by pinnipeds of the Wildlife Refuge of Ilha dos Lobos (WRIL), based on aerial photographic censuses. Twenty aerial photographic censuses were analysed between July 2010 and November 2018. To assess monthly differences in the numbers of pinnipeds in the WRIL we used a Generalized Linear Mixed Model. Spatial analysis was carried out using Kernel density analysis of the pinnipeds on a grid plotted along the WRIL. Subadult male South American sea lions (Otaria flavescens) were the most abundant pinniped in the WRIL. Potential females of this species were also recorded during half of the census. The maximum number of pinnipeds observed in the WRIL was 304 in September 2018, including an unexpected individual southern elephant seal (Mirounga leonina), and a high number of South American fur seal yearlings (Arctocephalus australis). However, there was no statistically significant difference in counts between months. In all months analysed, pinnipeds were most often found concentrated in the northern portion of the island, with the highest abundances reported in September. This study confirms the importance of the WRIL as a haulout site for pinnipeds in Brazil, recommends that land research and recreational activities occur in months when no pinnipeds are present, and encourages a regulated marine mammal-based tourism during winter and spring months.

Adaptations to a semiaquatic lifestyle in the external ear of southern pinnipeds (Otariidae and Phocidae, Carnivora): Morphological evidences.

Pinnipeds are semiaquatic carnivorans that spend most of their lives in water and use coastal terrestrial, or ice pack, environments to breed, molt and rest. Certain characteristics of the ear have been linked to ecological aspects. In our contribution we focus on the study of the macroscopic and microscopic morphology of the external ear (with the exception of the osseous outer ear canal) of six species of Southern pinnipeds. In order to recognize the different components of tissues, sections were stained following several routine protocols. In addition, double-staining and enzymatic clearing (Alcian blue-alizarin red) was performed to assess the arrangement of skeletal elements in the OEC. The basic structure of the pinna in the southern otariids studied match those previously analyzed for Northern Hemisphere species. The cartilage macro anatomy of the OEC of Mirounga leonina and Arctocephallus gazella is different from that of the Northern Hemisphere species, with only one plate of cartilage, but markedly different between them. The histology of the otariids OEC is homogeneous along the entire extension, but phocids has three different regions (distal, middle, and proximal). The cartilage histology of most phocids is also different from that of analyzed otariids, with an elastic cartilage that resembles a myxoid-like tissue, but is not present in M. leonina, were the tissue around the OEC is very rich in adipocytes. The southern elephant seal M. leonina OEC has a combination of features similar to both the rest of the phocids and to the otariids. An auditory organ that is functional both over and under water could be essential for social behavior in these species.

Flipper bone distribution reveals flexible trailing edge in underwater flying marine tetrapods.

Hydrofoil-shaped limbs (flipper-hydrofoils) have evolved independently several times in secondarily marine tetrapods and generally fall into two functional categories: (1) those that produce the majority of thrust during locomotion (propulsive flipper-hydrofoils); (2) those used primarily to steer and resist destabilizing movements such as yaw, pitch, and roll (controller flipper-hydrofoils). The morphological differences between these two types have been poorly understood. Theoretical and experimental studies on engineered hydrofoils suggest that flapping hydrofoils with a flexible trailing edge are more efficient at producing thrust whereas hydrofoils used in steering and stabilization benefit from a more rigid one. To investigate whether the trailing edge is generally more flexible in propulsive flipper-hydrofoils, we compared the bone distribution along the chord in both flipper types. The propulsive flipper-hydrofoil group consists of the forelimbs of Chelonioidea, Spheniscidae, and Otariidae. The controller flipper-hydrofoil group consists of the forelimbs of Cetacea. We quantified bone distribution from radiographs of species representing more than 50% of all extant genera for each clade. Our results show that the proportion of bone in both groups is similar along the leading edge (0-40% of the chord) but is significantly less along the trailing edge for propulsive flipper-hydrofoils (40-80% of the chord). Both flipper-hydrofoil types have little to no bony tissue along the very edge of the trailing edge (80-100% of the chord). This suggests a relatively flexible trailing edge for propulsive flipper-hydrofoils compared to controller flipper-hydrofoils in line with findings from prior studies. This study presents a morphological correlate for inferring flipper-hydrofoil function in extinct taxa and highlights the importance of a flexible trailing edge in the evolution of propulsive flipper-hydrofoils in marine tetrapods.

Empirical measures of harbor seal behavior and avoidance of an operational tidal turbine.

There is global interest in marine renewable energy from underwater tidal turbines. Due to overlap in animal habitat with locations for tidal turbines, the potential for collisions has led to concern around strike risk. Using data from tagged harbor seals collected before construction and after operation of the SeaGen tidal turbine in Northern Ireland, this study quantifies risks of an operational turbine to harbor seals by taking into account turbine characteristics, tidal state, and seal behavior. We found 68% spatial avoidance (95% C.I., 37%, 83%) by harbor seals within 200 m of the turbine. When additionally accounting for variation in seal occupancy over depth and tidal flows, there is an overall reduction in collision risk from 1.29 to 0.125 seals per tidal cycle (90.3% reduction; (95% C.I., 83%, 98%)) compared to risk calculated under assumptions of uniform habitat use. This demonstrates the need to incorporate environmental conditions to properly assess strike risk.

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.

Social relationships and death-related behaviour in aquatic mammals: a systematic review.

Some aquatic mammals appear to care for their dead, whereas others abandon their live offspring when conditions are unfavourable. This incredible variety in behaviours suggests the importance of comparing and contrasting mechanisms driving death-related behaviours among these species. We reviewed 106 cases of aquatic mammals (81 cetaceans and 25 non-cetaceans) reacting to a death event, and extrapolated 'participant' (age class, sex, relationship and decomposition) and 'social' characteristics (escorting, calf dependence, alloparental care, herding and dispersal patterns) from published and unpublished literature. A multiple correspondence analysis (MCA) was performed to explore the relationships between these characteristics and death-related behaviours, with species clustered based on MCA scores. Results showed that both cetaceans and non-cetaceans react to death but in different ways. Non-cetaceans, characterized by a short maternal investment, were observed to protect the dead (defending it from external attacks), while cetaceans spent much longer with their offspring and display carrying (hauling, spinning, mouthing with the carcass and diving with it) and breathing-related (lifting and sinking the carcass) activities with the dead generally in association with other conspecifics. Our work emphasizes the need of increased documentation of death-related cases around the world to improve our understanding of aquatic mammals and their responses to death.This article is part of the theme issue 'Evolutionary thanatology: impacts of the dead on the living in humans and other animals'.

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.

Ecotoxicoparasitology of the gastrointestinal tracts of pinnipeds: the effect of parasites on the potential bioavailability of total mercury (THg).

Acanthocephalans, cestodes, and some species of nematodes acquire nutrients from the lumen contents in the gastrointestinal (GI) tract of their definitive host. These parasites are exposed to toxicants, such as mercury (Hg), through passive or active feeding mechanisms; therefore, the focus of this study was to determine if there is an effect of parasites on the dietary availability of total mercury (THg) within piscivorous pinniped hosts. THg concentrations ([THg]) in selected host tissues, parasites, and GI lumen contents from 22 California sea lions (Zalophus californianus), 15 ringed seals (Phoca hispida), and 4 spotted seals (Phoca largha) were determined. Among all pinnipeds, [THg] in acanthocephalans of the large intestine were significantly higher than concentrations in other samples (host lumen contents, other parasites and host intestinal wall), irrespective of location within the host GI tract. δ15N values of parasites depended both on parasite group and location within the GI tract. δ15N values were consistently higher in parasites inhabiting the large intestine, compared to elsewhere in the GI tract, for both sea lions and seals. δ13C values in parasites did not differ significantly from host GI tissues. Based on both [THg] and stable isotope values, parasites are likely affecting the Hg bioavailability within the GI lumen contents and host tissues, and toxicant-parasite interactions appear to depend on both parasitic taxon as well as their location within the host intestine.

Fully 3D Printed Multi-Material Soft Bio-Inspired Whisker Sensor for Underwater-Induced Vortex Detection.

Bio-mimicking the underwater sensors has tremendous potential in soft robotics, under water exploration and human interfaces. Pinniped are semiaquatic carnivores that use their whiskers to sense food by tracking the vortices left by potential prey. To detect and track the vortices inside the water, a fully 3D printed pinniped inspired multi-material whisker sensor is fabricated and characterized. The fabricated whisker is composed of a polyurethane rod with a length-to-diameter ratio (L/d) of 20:1 with four graphene patterns (length × diameter: 60 × 0.3 mm) perpendicular to each other. The graphene patterns are further connected with output signal wires via copper tape. The displacement (∼5 mm) of the whisker rod in any direction (0-360°) causes the change in resistance [Formula: see text] because of generated tensile. The analog signals (resistance change) are digitalized by using analog to digital modules and fed to a microcontroller to detect the vortex. A virtual environment is designed such that it consists of a 3D printed fish fin, a water tank, a camera, and data loggers to study the response of fabricated whisker. The underwater sensitivity of the whisker sensor in any direction is detectable and remarkably high ([Formula: see text]% ∼1180). The mechanical reliability of the whisker sensor is tested by bending it up to 2000 cycles. The fabricated whisker's structure and material are unique, and no one has fabricated them by using cost-effective 3D printing methods earlier. This fully 3D printable flexible whisker sensor should be applicable to a wide range of soft robotic applications.

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.

Blood cadmium and metallothionein concentrations in females of two sympatric pinnipeds species.

Otaria flavescens (SASL) and Arctocephalus australis (SAFS) are endemic of South America. The aims were to assess Cd concentrations in red blood cells (RBC) and plasma from free living females of both species; and to establish metallothioneins (MT) levels in blood fractions and the possible relationship between MTs and Cd. Blood of fifteen SASL and eight SAFS females from Isla de Lobos were analyzed (years 2010-2011). All animals showed Cd levels above the detection limit. Cd concentrations on SAFS were higher than those of SASL, however, no significant differences were observed on metal concentrations between cell fractions by species. Metal levels were associated with a natural presence and ecological-trophic habits of the prey items. On SASL the MT concentrations between fractions were similar; whereas, SAFS plasma concentrations were higher than RBC. The results reported constitute the first information on Cd and MT blood levels in these species.

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 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.