A longitudinal study of endocrinology and foraging ecology of subadult gray whales prior to death based on baleen analysis.

Individual-level assessments of wild animal health, vital rates, and foraging ecology are critical for understanding population-wide impacts of exposure to stressors. Large whales face multiple stressors, including, but not limited to, ocean noise, pollution, and ship strikes. Because baleen is a continuously growing keratinized structure, serial extraction, and quantification of hormones and stable isotopes along the length of baleen provide a historical record of whale physiology and foraging ecology. Furthermore, baleen analysis enables the investigation of dead specimens, even decades later, allowing comparisons between historic and modern populations. Here, we examined baleen of five sub-adult gray whales and observed distinct patterns of oscillations in δ15N values along the length of their baleen plates which enabled estimation of baleen growth rates and differentiation of isotopic niche widths of the whales during wintering and summer foraging. In contrast, no regular patterns were apparent in δ13C values. Prolonged elevation of cortisol in four individuals before death indicates that chronic stress may have impacted their health and survival. Triiodothyronine (T3) increased over months in the whales with unknown causes of death, simultaneous with elevations in cortisol, but both hormones remained stable in the one case of acute death attributed to killer whale predation. This parallel elevation of cortisol and T3 challenges the classic understanding of their interaction and might relate to increased energetic demands during exposure to stressors. Reproductive hormone profiles in subadults did not show cyclical trends, suggesting they had not yet reached sexual maturity. This study highlights the potential of baleen analysis to retrospectively assess gray whales' physiological status, exposure to stressors, reproductive status, and foraging ecology in the months or years leading up to their death, which can be a useful tool for conservation diagnostics to mitigate unusual mortality events.

Geographic range size, water temperature, and extrinsic threats predict the extinction risk in global cetaceans.

Despite the fact that cetaceans provide significant ecological contributions to the health and stability of aquatic ecosystems, many are highly endangered with nearly one-third of species assessed as threatened with extinction. Nevertheless, to date, few studies have explicitly examined the patterns and processes of extinction risk and threats for this taxon, and even less between the two subclades (Mysticeti and Odontoceti). To fill this gap, we compiled a dataset of six intrinsic traits (active region, geographic range size, body weight, diving depth, school size, and reproductive cycle), six environmental factors relating to sea surface temperature and chlorophyll concentration, and two human-related threat indices that are commonly recognized for cetaceans. We then employed phylogenetic generalized least squares models and model selection to identify the key predictors of extinction risk in all cetaceans, as well as in the two subclades. We found that geographic range size, sea surface temperature, and human threat index were the most important predictors of extinction risk in all cetaceans and in odontocetes. Interestingly, maximum body weight was positively associated with the extinction risk in mysticetes, but negatively related to that for odontocetes. By linking seven major threat types to extinction risk, we further revealed that fisheries bycatch was the most common threat, yet the impacts of certain threats could be overestimated when considering all species rather than just threatened ones. Overall, we suggest that conservation efforts should focus on small-ranged cetaceans and species living in warmer waters or under strong anthropogenic pressures. Moreover, further studies should consider the threatened status of species when superimposing risk maps and quantifying risk severity. Finally, we emphasize that mysticetes and odontocetes should be conserved with different strategies, because their extinction risk patterns and major threat types are considerably different. For instance, large-bodied mysticetes and small-ranged odontocetes require special conservation priority.

Co-evolution of cerebral and cerebellar expansion in cetaceans.

Cetaceans possess brains that rank among the largest to have ever evolved, either in terms of absolute mass or relative to body size. Cetaceans have evolved these huge brains under relatively unique environmental conditions, making them a fascinating case study to investigate the constraints and selection pressures that shape how brains evolve. Indeed, cetaceans have some unusual neuroanatomical features, including a thin but highly folded cerebrum with low cortical neuron density, as well as many structural adaptations associated with acoustic communication. Previous reports also suggest that at least some cetaceans have an expanded cerebellum, a brain structure with wide-ranging functions in adaptive filtering of sensory information, the control of motor actions, and cognition. Here, we report that, relative to the size of the rest of the brain, both the cerebrum and cerebellum are dramatically enlarged in cetaceans and show evidence of co-evolution, a pattern of brain evolution that is convergent with primates. However, we also highlight several branches where cortico-cerebellar co-evolution may be partially decoupled, suggesting these structures can respond to independent selection pressures. Across cetaceans, we find no evidence of a simple linear relationship between either cerebrum and cerebellum size and the complexity of social ecology or acoustic communication, but do find evidence that their expansion may be associated with dietary breadth. In addition, our results suggest that major increases in both cerebrum and cerebellum size occurred early in cetacean evolution, prior to the origin of the major extant clades, and predate the evolution of echolocation.

The evolution of foraging capacity and gigantism in cetaceans.

The extant diversity and rich fossil record of cetaceans provides an extraordinary evolutionary context for investigating the relationship between form, function and ecology. The transition from terrestrial to marine ecosystems is associated with a complex suite of morphological and physiological adaptations that were required for a fully aquatic mammalian life history. Two specific functional innovations that characterize the two great clades of cetaceans, echolocation in toothed whales (Odontoceti) and filter feeding in baleen whales (Mysticeti), provide a powerful comparative framework for integrative studies. Both clades exhibit gigantism in multiple species, but we posit that large body size may have evolved for different reasons and in response to different ecosystem conditions. Although these foraging adaptations have been studied using a combination of experimental and tagging studies, the precise functional drivers and consequences of morphological change within and among these lineages remain less understood. Future studies that focus at the interface of physiology, ecology and paleontology will help elucidate how cetaceans became the largest predators in aquatic ecosystems worldwide.

Evolutionary aspects of the development of teeth and baleen in the bowhead whale.

In utero, baleen whales initiate the development of several dozens of teeth in upper and lower jaws. These tooth germs reach the bell stage and are sometimes mineralized, but toward the end of prenatal life they are resorbed and no trace remains after birth. Around the time that the germs disappear, the keratinous baleen plates start to form in the upper jaw, and these form the food-collecting mechanism. Baleen whale ancestors had two generations of teeth and never developed baleen, and the prenatal teeth of modern fetuses are usually interpreted as an evolutionary leftover. We investigated the development of teeth and baleen in bowhead whale fetuses using histological and immunohistochemical evidence. We found that upper and lower dentition initially follow similar developmental pathways. As development proceeds, upper and lower tooth germs diverge developmentally. Lower tooth germs differ along the length of the jaw, reminiscent of a heterodont dentition of cetacean ancestors, and lingual processes of the dental lamina represent initiation of tooth bud formation of replacement teeth. Upper tooth germs remain homodont and there is no evidence of a secondary dentition. After these germs disappear, the oral epithelium thickens to form the baleen plates, and the protein FGF-4 displays a signaling pattern reminiscent of baleen plates. In laboratory mammals, FGF-4 is not involved in the formation of hair or palatal rugae, but it is involved in tooth development. This leads us to propose that the signaling cascade that forms teeth in most mammals has been exapted to be involved in baleen plate ontogeny in mysticetes.

Development of a Model to Assess Masking Potential for Marine Mammals by the Use of Air Guns in Antarctic Waters.

We estimated the long-range effects of air gun array noise on marine mammal communication ranges in the Southern Ocean. Air gun impulses are subject to significant distortion during propagation, potentially resulting in a quasi-continuous sound. Propagation modeling to estimate the received waveform was conducted. A leaky integrator was used as a hearing model to assess communication masking in three species due to intermittent/continuous air gun sounds. Air gun noise is most probably changing from impulse to continuous noise between 1,000 and 2,000 km from the source, leading to a reduced communication range for, e.g., blue and fin whales up to 2,000 km from the source.

A comparative analysis of cone photoreceptor morphology in bowhead and beluga whales.

The cetacean visual system is a product of selection pressures favoring underwater vision, yet relatively little is known about it across taxa. Previous studies report several mutations in the opsin genetic sequence in cetaceans, suggesting the evolutionary complete or partial loss of retinal cone photoreceptor function in mysticete and odontocete lineages, respectively. Despite this, limited anatomical evidence suggests cone structures are partially maintained but with absent outer and inner segments in the bowhead retina. The functional consequence and anatomical distributions associated with these unique cone morphologies remain unclear. The current study further investigates the morphology and distribution of cone photoreceptors in the bowhead whale and beluga retina and evaluates the potential functional capacity of these cells' alternative to photoreception. Refined histological and advanced microscopic techniques revealed two additional cone morphologies in the bowhead and beluga retina that have not been previously described. Two proteins involved in magnetosensation were present in these cone structures suggesting the possibility for an alternative functional role in responding to changes in geomagnetic fields. These findings highlight a revised understanding of the unique evolution of cone and gross retinal anatomy in cetaceans, and provide prefatory evidence of potential functional reassignment of these cells.

Prenatal Development of the Humpback Whale: Growth Rate, Tooth Loss and Skull Shape Changes in an Evolutionary Framework.

Extant baleen whales (Mysticeti) share a distinct suite of extreme and unique adaptations to perform bulk filter feeding, such as a long, arched skull, and mandible and the complete loss of adult dentition in favor of baleen plates. However, mysticetes still develop tooth germs during ontogeny. In the fossil record, multiple groups document the transition from ancestral raptorial feeding to filter feeding. Fetal specimens give us an extraordinary opportunity to observe when and how this macroevolutionary transition occurs during gestation. We used iodine-enhanced and traditional CT scanning to visualize the internal anatomy of five fetuses of humpback whale representing the first two-thirds of gestation, and we combine these data with previously published reports to provide the first comprehensive qualitative description of the sequence of developmental changes that characterize the skull and dentition. We also use quantitative methods based on 3D landmarks to investigate the shape changes in the fetuses in relation to a juvenile cranial morphology. We found similarities in the ossification patterns of the humpback and other cetaceans (dolphins), but there appear to be major differences when comparing them to terrestrial artiodactyls. As for the tooth germs, this developmental sequence confirms that the tooth-to-baleen transition occurs in the last one-third of gestation. Analysis of cranial shape development revealed a progressive elongation of the rostrum and a resulting posterior movement of the nasals relative to the braincase. Future work will involve acquisition of data from other species to complete our documentation of the teeth-to-baleen transition. Anat Rec, 2018. © 2018 American Association for Anatomy.

Comparative Three-Dimensional Morphology of Baleen: Cross-Sectional Profiles and Volume Measurements Using CT Images.

Baleen whales are obligate filter feeders, straining prey-laden seawater through racks of keratinized baleen plates. Despite the importance of baleen to the ecology and natural history of these animals, relatively little work has been done on baleen morphology, particularly with regard to the three-dimensional morphology and structure of baleen. We used computed tomography (CT) scanning to take 3D images of six baleen specimens representing five species, including three complete racks. With these images, we described the three-dimensional shape of the baleen plates using cross-sectional profiles from within the gum tissue to the tip of the plates. We also measured the percentage of each specimen that was composed of either keratinized plate material or was void space between baleen plates, and thus available for seawater flow. Baleen plates have a complex three-dimensional structure with curvature that varies across the anterior-posterior, proximal-distal, and medial-lateral (lingual-labial) axes. These curvatures also vary with location along the baleen rack, and between species. Cross-sectional profiles resemble backwards-facing airfoils, and some specimens display S-shaped, or reflexed, camber. Within a baleen specimen, the intra-baleen void volume correlates with the average bristle diameter for a species, suggesting that essentially, thinner plates (with more space between them for flow) have thinner bristles. Both plate curvature and the relative proportions of plate and void volumes are likely to have implications for the mechanics of mysticete filtration, and future studies are needed to determine the particular functions of these morphological characters. Anat Rec, 300:1942-1952, 2017. © 2017 The Authors The Anatomical Record published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.