How do marine mammals manage and usually avoid gas emboli formation and gas embolic pathology? critical clues from studies of wild dolphins

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fahlman, A., Moore, M. J., & Wells, R. S. How do marine mammals manage and usually avoid gas emboli formation and gas embolic pathology? critical clues from studies of wild dolphins. Frontiers in Marine Science, 8, (2021): 598633, https://doi.org/10.3389/fmars.2021.598633.Decompression theory has been mainly based on studies on terrestrial mammals, and may not translate well to marine mammals. However, evidence that marine mammals experience gas bubbles during diving is growing, causing concern that these bubbles may cause gas emboli pathology (GEP) under unusual circumstances. Marine mammal management, and usual avoidance, of gas emboli and GEP, or the bends, became a topic of intense scientific interest after sonar-exposed, mass-stranded deep-diving whales were observed with gas bubbles. Theoretical models, based on our current understanding of diving physiology in cetaceans, predict that the tissue and blood N2 levels in the bottlenose dolphin (Tursiops truncatus) are at levels that would result in severe DCS symptoms in similar sized terrestrial mammals. However, the dolphins appear to have physiological or behavioral mechanisms to avoid excessive blood N2 levels, or may be more resistant to circulating bubbles through immunological/biochemical adaptations. Studies on behavior, anatomy and physiology of marine mammals have enhanced our understanding of the mechanisms that are thought to prevent excessive uptake of N2. This has led to the selective gas exchange hypothesis, which provides a mechanism how stress-induced behavioral change may cause failure of the normal physiology, which results in excessive uptake of N2, and in extreme cases may cause formation of symptomatic gas emboli. Studies on cardiorespiratory function have been integral to the development of this hypothesis, with work initially being conducted on excised tissues and cadavers, followed by studies on anesthetized animals or trained animals under human care. These studies enabled research on free-ranging common bottlenose dolphins in Sarasota Bay, FL, and off Bermuda, and have included work on the metabolic and cardiorespiratory physiology of both shallow- and deep-diving dolphins and have been integral to better understand how cetaceans can dive to extreme depths, for long durations.Many of the studies that have resulted in the data in this review, and that have been integral to develop the selective gas exchange hypothesis have been funded by the Office of Naval Research (ONR Awards # N000141010159, N000141613088, N000141410563, N000140811220, and ONR YIP Award # N000141410563), and Dolphin Quest. The authors declare that Dolphin Quest was not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication

Democracy and Dysfunction: Rural Electric Cooperatives and the Surprising Persistence of the Separation of Ownership and Control

Since the 1930s, corporate law scholarship has focused narrowly on the public corporation and the problem of the separation of ownership and control-a problem many now believe has been mitigated or even solved. With rare exceptions, scholars have paid far less heed to other business forms that still play important roles in the American economy. In this Article, we examine a significant and almost completely overlooked business form, the Rural Electric Cooperative (REC). RECs were founded in a moment of optimism during the New Deal. As with other cooperatives, their organizational rules differed sharply from those of for-profit corporations. They were owned by their customers, with each customer-member having one vote irrespective of their energy consumption, and it was hoped these owners would provide active oversight of the REC\u27s managers and activities. Reality has proven otherwise. Corporate governance innovations of the last forty years have passed RECs by, leaving an organizational sector mired in governance dysfunctions stemming from the separation of ownership and control. Here we explain why RECs evolved as they did and why New Deal planners seized on the cooperative form to electrify the countryside; how significant governance problems have persisted, largely unaddressed, from the 1930s to today; and how a change in corporate governance rules, allowing for a market for corporate control in RECs, could fix some persistent problems in this still-important sector. Alternatively, we propose that RECs take up a new public role as rural broadband internet providers with a reinvigorated federal regulator to police governance failures

Identifying signature whistles from recordings of groups of unrestrained bottlenose dolphins (Tursiops truncatus)

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Marine Mammal Science 29 (2013): 109–122, doi:10.1111/j.1748-7692.2011.00549.x.Bottlenose dolphins (Tursiops truncatus) have individually-distinctive signature whistles. Each individual dolphin develops its own unique frequency modulation pattern and uses it to broadcast its identity. However, underwater sound localization is challenging, and researchers have had difficulties identifying signature whistles. The traditional method to identify them involved isolating individuals. In this context, the signature whistle is the most commonly produced whistle type of an animal. However, most studies on wild dolphins cannot isolate animals. We present a novel method, SIGID, that can identify signature whistles in recordings of groups of dolphins recorded via a single hydrophone. We found that signature whistles tend to be delivered in bouts with whistles of the same type occurring within 1-10 s of each other. Non-signature whistles occur over longer or shorter periods, and this distinction can be used to identify signature whistles in a recording. We tested this method on recordings from wild and captive bottlenose dolphins and show thresholds needed to identify signature whistles reliably. SIGID will facilitate the study of signature whistle use in the wild, signature whistle diversity between different populations, and potentially allow signature whistles to be used in mark-recapture studies.This work was supported by Dolphin Quest, National Oceanic and Atmospheric Administration (NOAA) Fisheries Service, Disney’s Animal Programs and Mote Marine Laboratory (R.S.W.), Harbor Branch Oceanographic Institute (L.S.S. and R.S.W.), and a Royal Society University Research Fellowship (V.M.J.)

Genome sequence of a gammaherpesvirus from a common bottlenose dolphin (Tursiops truncatus)

A herpesvirus genome was sequenced directly from a biopsy specimen of a rectal lesion from a female common bottlenose dolphin. This genome sequence comprises a unique region (161,235 bp) flanked by multiple copies of a terminal repeat (4,431 bp) and contains 72 putative genes. The virus was named common bottlenose dolphin gammaherpesvirus 1

The Bottlenose Dolphin Epigenetic Aging Tool (BEAT): A Molecular Age Estimation Tool for Small Cetaceans

Age constitutes a critical parameter for the study of animal populations, providing information about development, environmental effects, survival, and reproduction. Unfortunately, age estimation is not only challenging in large, mobile and legally protected species, but often involves invasive sampling methods. The present work investigates the association between epigenetic modifications and chronological age in small cetaceans. For that purpose, DNA methylation at age-linked genes was characterized in an extensively studied, long-term resident common bottlenose dolphin (Tursiops truncatus) community from Sarasota Bay (FL, United States) for which sampled individuals have a known age. Results led to the identification of several CpG sites that are significantly correlated to chronological age in this species with the potential for sex to play a role in the modulation of this correlation. These findings have allowed for the development and validation of the “Bottlenose dolphin Epigenetic Age estimation Tool” (BEAT), improving minimally-invasive age estimation in free-ranging small cetaceans. Overall, the BEAT proved to be accurate in estimating age in these organisms. Given its minimally-invasive nature and potential large-scale implementation using skin biopsy samples, this tool can be used to generate age data from free-ranging small cetacean populations

Parameterizing animal sounds and motion with animal-attached tags to study acoustic communication

Funding: Dolphin Quest, Inc.; School of Biology, University of St Andrews; Scottish Universities Life Sciences Alliance; Office of Naval Research; Marine Alliance for Science and Technology for Scotland; Horizon H2020.Stemming from the traditional use of field observers to score states and events, the study of animal behaviour often relies on analyses of discrete behavioural categories. Many studies of acoustic communication record sequences of animal sounds, classify vocalizations, and then examine how call categories are used relative to behavioural states and events. However, acoustic parameters can also convey information independent of call type, offering complementary study approaches to call classifications. Animal-attached tags can continuously sample high-resolution behavioural data on sounds and movements, which enables testing how acoustic parameters of signals relate to parameters of animal motion. Here, we present this approach through case studies on wild common bottlenose dolphins (Tursiops truncatus). Using data from sound-and-movement recording tags deployed in Sarasota (FL), we parameterized dolphin vocalizations and motion to investigate how senders and receivers modified movement parameters (including vectorial dynamic body acceleration, “VeDBA”, a proxy for activity intensity) as a function of signal parameters. We show that (1) VeDBA of one female during consortships had a negative relationship with centroid frequency of male calls, matching predictions about agonistic interactions based on motivation-structural rules; (2) VeDBA of four males had a positive relationship with modulation rate of their pulsed vocalizations, confirming predictions that click-repetition rate of these calls increases with agonism intensity. Tags offer opportunities to study animal behaviour through analyses of continuously sampled quantitative parameters, which can complement traditional methods and facilitate research replication. Our case studies illustrate the value of this approach to investigate communicative roles of acoustic parameter changes.Publisher PDFPeer reviewe

Bottlenose dolphin mothers modify signature whistles in the presence of their own calves

PLT received support from ONR grants N00014-18-1-2062 and N00014-20-1-2709. Financial support for the whistle database project has come from the Protect Wild Dolphins fund at Harbor Branch Oceanographic Institute, Vulcan Machine Learning Center for Impact, Allen Institute for Artificial Intelligence, Adelaide M. & Charles B. Link Foundation, and Dolphin Quest, Inc.Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this “motherese,” or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother–offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.Publisher PDFPeer reviewe

Signal-specific amplitude adjustment to noise in common bottlenose dolphins (Tursiops truncatus)

Fieldwork in Sarasota was funded by the Grossman Foundation, the Office of Naval Research, and Woods Hole Oceanographic Institution. Health assessments were funded by Dolphin Quest, Inc. I.M.K. received support from the Danish Acoustical Society (Dansk Akustisk Selskab). P.L.T. received funding from the University of St Andrews, the Office of Naval Research (N00014-19-1-2560) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). F.H.J. was supported by the Office of Naval Research (N00014-1410410) and an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the FP7-PEOPLE programme of the EU (agreement no. 609033). All support is gratefully acknowledged.Anthropogenic underwater noise has increased over the past century, raising concern about the impact on cetaceans that rely on sound for communication, navigation and locating prey and predators. Many terrestrial animals increase the amplitude of their acoustic signals to partially compensate for the masking effect of noise (the Lombard response), but it has been suggested that cetaceans almost fully compensate with amplitude adjustments for increasing noise levels. Here, we used sound-recording DTAGs on pairs of free-ranging common bottlenose dolphins (Tursiops truncatus) to test (i) whether dolphins increase signal amplitude to compensate for increasing ambient noise and (ii) whether adjustments are identical for different signal types. We present evidence of a Lombard response in the range 0.1–0.3 dB per 1 dB increase in ambient noise, which is similar to that of terrestrial animals, but much lower than the response reported for other cetaceans. We found that signature whistles tended to be louder and with a lower degree of amplitude adjustment to noise compared with non-signature whistles, suggesting that signature whistles may be selected for higher output levels and may have a smaller scope for amplitude adjustment to noise. The consequence of the limited degree of vocal amplitude compensation is a loss of active space during periods of increased noise, with potential consequences for group cohesion, conspecific encounter rates and mate attraction.Publisher PDFPeer reviewe