Gross and histological morphology of the cervical gill slit gland of the pygmy sperm whale (Kogia breviceps).

Odontocete cetaceans have undergone profound modifications to their integument and sensory systems and are generally thought to lack specialized exocrine glands that in terrestrial mammals function to produce chemical signals (Thewissen & Nummela, 2008). Keenan-Bateman et al. (2016, 2018), though, introduced an enigmatic exocrine gland, associated with the false gill slit pigmentation pattern in Kogia breviceps. These authors provided a preliminary description of this cervical gill slit gland in their helminthological studies of the parasitic nematode, Crassicauda magna. This study offers the first detailed gross and histological description of this gland and reports upon key differences between immature and mature individuals. Investigation reveals it is a complex, compound tubuloalveolar gland with a well-defined duct that leads to a large, and expandable central chamber, which in turn leads to two caudally projecting diverticula. All regions of the gland contain branched tubular and alveolar secretory regions, although most are found in the caudal diverticula, where the secretory process is holocrine. The gland lies between slips of cutaneous muscle, and is innervated by lamellar corpuscles, resembling Pacinian's corpuscles, suggesting that its secretory product may be actively expressed into the environment. Mature K. breviceps display larger gland size, and increased functional activity in glandular tissues, as compared to immature individuals. These results demonstrate that the cervical gill slit gland of K. breviceps shares morphological features of the specialized, chemical signaling, exocrine glands of terrestrial members of the Cetartiodactyla.

Evidence of multi-decadal behavior and ecosystem-level changes revealed by reconstructed lifetime stable isotope profiles of baleen whale earplugs.

Biological time series datasets provide an unparalleled opportunity to investigate regional and global changes in the marine environment. Baleen whales are long-lived sentinel species and an integral part of the marine ecosystem. Increasing anthropogenic terrestrial and marine activities alter ocean systems, and such alterations could change foraging and feeding behavior of baleen whales. In this study, we analyzed δ13C and δ15N of baleen whale earplugs from three different species (N = 6 earplugs, n = 337 laminae) to reconstruct the first continuous stable isotope profiles with a six-month resolution. Results of our study provide an unprecedented opportunity to assess behavioral as well as ecological changes. Abrupt shifts and temporal variability observed in δ13C and δ15N profiles could be indicative of behavior change such as shift in foraging location and/or trophic level in response to natural or anthropogenic disturbances. Additionally, five out of six individuals demonstrated long-term declining trends in δ13C profiles, which could suggest influence of emission of depleted 13CO2 from fossil fuel combustion referred to as the Suess effect. After adjusting the δ13C values of earplugs for the estimated Suess effect and re-evaluating δ13C profiles, significant decline in δ13C values as well as different rate of depletion suggest contribution of other sources that could impact δ13C values at the base of the food web.

Hormone comparison between right and left baleen whale earplugs.

Marine animals experience additional stressors as humans continue to industrialize the oceans and as the climate continues to rapidly change. To examine how the environment or humans impact animal stress, many researchers analyse hormones from biological matrices. Scientists have begun to examine hormones in continuously growing biological matrices, such as baleen whale earwax plugs, baleen and pinniped vibrissae. Few of these studies have determined if the hormones in these tissues across the body of the organism are interchangeable. Here, hormone values in the right and left earplugs from the same individual were compared for two reasons: (i) to determine whether right and left earplug hormone values can be used interchangeably and (ii) to assess methods of standardizing hormones in right and left earplugs to control for individuals' naturally varying hormone expressions. We analysed how absolute, baseline-corrected and Z-score normalized hormones performed in reaching these goals. Absolute hormones in the right and left earplugs displayed a positive relationship, while using Z-score normalization was necessary to standardize the variance in hormone expression. After Z-score normalization, it was possible to show that the 95% confidence intervals of the differences in corresponding lamina of the right and left earplugs include zero for both cortisol and progesterone. This indicates that the hormones in corresponding lamina of right and left earplugs are no different from zero. The results of this study reveal that both right and left earplugs from the same baleen whale can be used in hormone analyses after Z-score normalization. This study also shows the importance of Z-score normalization to interpretation of results and methodologies associated with analysing long-term trends using whale earplugs.

Eighty years of chemical exposure profiles of persistent organic pollutants reconstructed through baleen whale earplugs.

Despite decades of effort, significant knowledge gaps still exist regarding the global transport and distribution of persistent organic pollutants (POPs) in marine ecosystems, especially for periods prior to the 1970s. Furthermore, for long-lived marine mammals such as baleen whales, POPs impacts on early developmental (first years of life), as well as lifetime exposure profiles for periods of use and phase-out, are not well characterized. Recently, analytical techniques capable of reconstructing lifetime (i.e., birth to death; ~6 mos. resolution) chemical exposure profiles in baleen whale earplugs have been developed. Earplugs represent a unique opportunity to examine the spatiotemporal trends of POPs in the marine ecosystem. Baleen whale earplugs were collected from six whales (one blue whale (Balaenoptera musculus) and five fin whales (Balaenoptera physalus)), including four from archived collections and two from recent strandings. Lifespans for some of these individuals date back to the 1930s and provide insight into early periods of POP use. POP concentrations (reported in ng g-1 dry wt.) were determined in laminae (n = 35) and were combined with age estimates and calendar year to reconstruct lifetime POP exposure profiles and lifetime bioaccumulation rates. Dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCBs) were found to be the most dominant POPs (spanning the past 80 y), were detected as early as the 1930s and were ubiquitous in the North Pacific and Atlantic Oceans. Lifetime bioaccumulation rates determined using baleen whale earplugs were 56 times higher in the North Pacific as compared to the North Atlantic. This suggest baleen whales from the North Pacific may be to be exposed to increased levels of POPs.

The complete mitochondrial genome of the critically endangered Atlantic humpback dolphin, Sousa teuszii (Kükenthal, 1892).

The Atlantic humpback dolphin remains an understudied, critically endangered cetacean species. Here, we describe the first complete mitogenome of Sousa teuszii, derived from an animal stranded on Île des Oiseaux, Sine Saloum, Senegal. The S. teuszii mitogenome is composed of 16,384 base pairs and is 98.1% identical to its closest relative with a mitogenome, Sousa chinensis. Phylogenetic analysis confirms its placement with S. chinensis, as well as the placement of the genus Sousa within subfamily Delphininae.

Baleen whale cortisol levels reveal a physiological response to 20th century whaling.

One of the most important challenges researchers and managers confront in conservation ecology is predicting a population's response to sub-lethal stressors. Such predictions have been particularly elusive when assessing responses of large marine mammals to past anthropogenic pressures. Recently developed techniques involving baleen whale earplugs combine age estimates with cortisol measurements to assess spatial and temporal stress/stressor relationships. Here we show a relationship between baseline-corrected cortisol levels and corresponding whaling counts of fin, humpback, and blue whales in the Northern Hemisphere spanning the 20th century. We also model the impact of alternative demographic and environmental factors and determine that increased anomalies of sea surface temperature over a 46-year mean (1970-2016) were positively associated with cortisol levels. While industrial whaling can deplete populations by direct harvest, our data underscore a widespread stress response in baleen whales that is peripheral to whaling activities or associated with other anthropogenic change.

Habitat use pattern of the giant parasitic nematode Crassicauda magna within the pygmy sperm whale Kogia breviceps.

The giant (>3 m) parasitic nematode Crassicauda magna infects kogiid whales, although only 3 studies to date have provided detailed descriptions of these worms, all based upon fragmented specimens. These fragments were found within the neck region of kogiids, an unusual anatomic site for this genus of parasites. C. magna is a species-specific parasite among kogiids, infecting only pygmy sperm whales Kogia breviceps, and with a primarily cervico-thoracic distribution. To date, however, the pattern of habitat use within the host and transmission path of this parasite remain unknown. We used detailed dissections (n = 12), histological examination of host tissues (n = 2), and scanning electron microscopy of excised nematodes (n = 7) to enhance our understanding of this host-parasite relationship. Results revealed that a critical habitat for the parasite is an exocrine gland in the whale's ventral cervical region. C. magna male and female tails were found intertwined within the glandular lumen, and eggs were observed within its presumed secretion, illuminating the transmission path out of the host. The cephalic ends of these worms were often meters away (curvilinearly), embedded deeply within epaxial muscle. A single worm's complete, tortuous 312 cm course, from the gland to its termination in the contralateral epaxial muscle, is described for the first time. This study also provides the first scanning electron micrographs of C. magna, which illustrate taxonomically important features of the heads and tails of both male and female worms.

Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology.

Extinctions and declines of large marine vertebrates have major ecological impacts and are of critical concern in marine environments. The Caribbean monk seal, Monachus tropicalis, last definitively reported in 1952, was one of the few marine mammal species to become extinct in historical times. Despite its importance for understanding the evolutionary biogeography of southern phocids, the relationships of M. tropicalis to the two living species of critically endangered monk seals have not been resolved. In this study we present the first molecular data for M. tropicalis, derived from museum skins. Phylogenetic analysis of cytochrome b sequences indicates that M. tropicalis was more closely related to the Hawaiian rather than the Mediterranean monk seal. Divergence time estimation implicates the formation of the Panamanian Isthmus in the speciation of Caribbean and Hawaiian monk seals. Molecular, morphological and temporal divergence between the Mediterranean and "New World monk seals" (Hawaiian and Caribbean) is profound, equivalent to or greater than between sister genera of phocids. As a result, we classify the Caribbean and Hawaiian monk seals together in a newly erected genus, Neomonachus. The two genera of extant monk seals (Monachus and Neomonachus) represent old evolutionary lineages each represented by a single critically endangered species, both warranting continuing and concerted conservation attention and investment if they are to avoid the fate of their Caribbean relative.

Sensory ability in the narwhal tooth organ system.

The erupted tusk of the narwhal exhibits sensory ability. The hypothesized sensory pathway begins with ocean water entering through cementum channels to a network of patent dentinal tubules extending from the dentinocementum junction to the inner pulpal wall. Circumpulpal sensory structures then signal pulpal nerves terminating near the base of the tusk. The maxillary division of the fifth cranial nerve then transmits this sensory information to the brain. This sensory pathway was first described in published results of patent dentinal tubules, and evidence from dissection of tusk nerve connection via the maxillary division of the fifth cranial nerve to the brain. New evidence presented here indicates that the patent dentinal tubules communicate with open channels through a porous cementum from the ocean environment. The ability of pulpal tissue to react to external stimuli is supported by immunohistochemical detection of neuronal markers in the pulp and gene expression of pulpal sensory nerve tissue. Final confirmation of sensory ability is demonstrated by significant changes in heart rate when alternating solutions of high-salt and fresh water are exposed to the external tusk surface. Additional supporting information for function includes new observations of dentinal tubule networks evident in unerupted tusks, female erupted tusks, and vestigial teeth. New findings of sexual foraging divergence documented by stable isotope and fatty acid results add to the discussion of the functional significance of the narwhal tusk. The combined evidence suggests multiple tusk functions may have driven the tooth organ system's evolutionary development and persistence.

Blue whale earplug reveals lifetime contaminant exposure and hormone profiles.

Lifetime contaminant and hormonal profiles have been reconstructed for an individual male blue whale (Balaenoptera musculus, Linnaeus 1758) using the earplug as a natural aging matrix that is also capable of archiving and preserving lipophilic compounds. These unprecedented lifetime profiles (i.e., birth to death) were reconstructed with a 6-mo resolution for a wide range of analytes including cortisol (stress hormone), testosterone (developmental hormone), organic contaminants (e.g., pesticides and flame retardants), and mercury. Cortisol lifetime profiles revealed a doubling of cortisol levels over baseline. Testosterone profiles suggest this male blue whale reached sexual maturity at approximately 10 y of age, which corresponds well with and improves on previous estimates. Early periods of the reconstructed contaminant profiles for pesticides (such as dichlorodiphenyltrichloroethanes and chlordanes), polychlorinated biphenyls, and polybrominated diphenyl ethers demonstrate significant maternal transfer occurred at 0-12 mo. The total lifetime organic contaminant burden measured between the earplug (sum of contaminants in laminae layers) and blubber samples from the same organism were similar. Total mercury profiles revealed reduced maternal transfer and two distinct pulse events compared with organic contaminants. The use of a whale earplug to reconstruct lifetime chemical profiles will allow for a more comprehensive examination of stress, development, and contaminant exposure, as well as improve the assessment of contaminant use/emission, environmental noise, ship traffic, and climate change on these important marine sentinels.

Vestigial tooth anatomy and tusk nomenclature for monodon monoceros.

Narwhal tusks, although well described and characterized within publications, are clouded by contradictory references, which refer to them as both incisors and canines. Vestigial teeth are briefly mentioned in the scientific literature with limited descriptions and no image renderings. This study first examines narwhal maxillary osteoanatomy to determine whether the erupted tusks are best described as incisiform or caniniform teeth. The study also offers evidence to support the evolutionary obsolescence of the vestigial teeth through anatomic, morphologic, and histologic descriptions. Examination of 131 skull samples, including 110 museum skull specimens and 21 harvested skulls, revealed the erupted tusks surrounded by maxillary bone over the entire length of their bone socket insertion, and are thus more accurately termed caniniform or canine teeth. The anatomy, morphology, and development of vestigial teeth in five skull samples are more fully described and documented. Vestigial tooth samples included 14 embedded pairs or individual teeth that were partially exposed or removed from the maxillary bone. Their location was posterior, ventral, and lateral to the tusks, although male vestigial teeth often exfoliate in the mouth lodging between the palatal tissue and underlying maxillary bone. Their myriad morphologies, sizes, and eruption patterns suggest that these teeth are no longer guided by function but rather by random germ cell differentiation and may eventually cease expression entirely. The conclusions reached are that the narwhal tusks are the expression of canine teeth and that vestigial teeth have no apparent functional characteristics and are following a pattern consistent with evolutionary obsolescence.