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ArticleRespiration cycle duration and seawater flux through open blowholes of humpback (Megaptera novaeangliae) and North Atlantic right (Eubalaena glacialis) whales(Wiley, 2020-05-29) Martins, Maria Clara Iruzun ; Miller, Carolyn ; Hamilton, Philip K. ; Robbins, Jooke ; Zitterbart, Daniel ; Moore, Michael J.Little is known about the dynamics of baleen whale respiratory cycles, especially the mechanics and activity of the blowholes and their interaction with seawater. In this study, the duration of complete respiration cycles (expiration/inhalation events) were quantified for the first time in two species: North Atlantic right whale (NARW) and humpback whale (HW) using high resolution, detailed imagery from an unoccupied aerial system (UAS). The mean duration of complete respiration cycles (expiration/inhalation event) in the NARW and HW were 3.07 s (SD = 0.503, n = 15) and 2.85 s (SD = 0.581, n = 21), respectively. Furthermore, we saw no significant differences in respiration cycle duration between age and sex classes in the NARW, but significant differences were observed between age classes in the HW. The observation of seawater covering an open blowhole was also quantified, with NARW having 20% of all breaths with seawater presence versus 90% in HW. Seawater incursion has not been described previously and challenges the general consensus that water does not enter the respiratory tract in baleen whales. Prevalent seawater has implications for the analysis and interpretation of exhaled respiratory vapor/mucosa samples, as well as for the potential inhalation of oil in spills.
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PresentationDon’t assume it’s ghost gear : accurate gear characterization is critical for entanglement mitigation [poster](Woods Hole Oceanographic Institution, 2017-10-25) Henry, Allison G. ; Barco, Susan G. ; Cole, Tim ; Johnson, Amanda ; Knowlton, Amy R. ; Landry, Scott ; Mattila, David K. ; Moore, Michael J. ; Robbins, Jooke ; van der Hoop, Julie ; Asmutis-Silvia, ReginaEntanglement is a significant conservation and welfare issue which is limiting the recovery of a number of marine species, including marine mammals. It is therefore important to reliably identify the causes of these events, including the nature of the entangling gear in order to reduce or prevent them in the future. A recently published review of marine debris assessed 76 publications and attributed a total of 1805 cases of cetacean entanglements in “ghost gear”, of which 78% (n=1413) were extracted from 13 peer reviewed publications. We examined the 13 publications cited in the review and found that the specific gear type or status of gear involved in the reported events was rarely mentioned beyond the fact that it was fishing related. This is likely due to the fact that determinations of debris as the entangling material are very difficult. In fact, in reviewing 10 years of large whale entanglement records for the U.S., the authors of another study reported that Hawaii was the only region in which any entangling gear was positively identified as ghost gear. The assumption that entangling gear is marine debris unless otherwise stated is dangerous because it could impact efforts to modify or restrict risk-prone fishing in key marine mammal habitats. Entanglement in actively fished gear poses a very real threat, and claims that only lost or abandoned fishing gear is responsible for entanglements can undermine conservation efforts.
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ArticleCharacterizing the culturable surface microbiomes of diverse marine animals(Oxford University Press, 2021-03-03) Keller, Abigail G. ; Apprill, Amy ; Lebaron, Philippe ; Robbins, Jooke ; Romano, Tracy ; Overton, Ellysia ; Rong, Yuying ; Yuan, Ruiyi ; Pollara, Scott B. ; Whalen, Kristen E.Biofilm-forming bacteria have the potential to contribute to the health, physiology, behavior and ecology of the host and serve as its first line of defense against adverse conditions in the environment. While metabarcoding and metagenomic information furthers our understanding of microbiome composition, fewer studies use cultured samples to study the diverse interactions among the host and its microbiome, as cultured representatives are often lacking. This study examines the surface microbiomes cultured from three shallow-water coral species and two whale species. These unique marine animals place strong selective pressures on their microbial symbionts and contain members under similar environmental and anthropogenic stress. We developed an intense cultivation procedure, utilizing a suite of culture conditions targeting a rich assortment of biofilm-forming microorganisms. We identified 592 microbial isolates contained within 15 bacterial orders representing 50 bacterial genera, and two fungal species. Culturable bacteria from coral and whale samples paralleled taxonomic groups identified in culture-independent surveys, including 29% of all bacterial genera identified in the Megaptera novaeangliae skin microbiome through culture-independent methods. This microbial repository provides raw material and biological input for more nuanced studies which can explore how members of the microbiome both shape their micro-niche and impact host fitness.
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ArticleBaleen whales are not important as prey for killer whales Orcinus orca in high-latitude regions(Inter-Research, 2007-10-25) Mehta, Amee V. ; Allen, Judith M. ; Constantine, Rochelle ; Garrigue, Claire ; Jann, Beatrice ; Jenner, Curt ; Marx, Marilyn K. ; Matkin, Craig O. ; Mattila, David K. ; Minton, Gianna ; Mizroch, Sally A. ; Olavarría, Carlos ; Robbins, Jooke ; Russell, Kirsty G. ; Seton, Rosemary E. ; Steiger, Gretchen H. ; Víkingsson, Gísli A. ; Wade, Paul R. ; Witteveen, Briana H. ; Clapham, Phillip J.Certain populations of killer whales Orcinus orca feed primarily or exclusively on marine mammals. However, whether or not baleen whales represent an important prey source for killer whales is debatable. A hypothesis by Springer et al. (2003) suggested that overexploitation of large whales by industrial whaling forced killer whales to prey-switch from baleen whales to pinnipeds and sea otters, resulting in population declines for these smaller marine mammals in the North Pacific and southern Bering Sea. This prey-switching hypothesis is in part contingent upon the idea that killer whales commonly attack mysticetes while they are in these high-latitude areas. In this study, we used photographic and sighting data from long-term studies of baleen whales in 24 regions worldwide to determine the proportion of whales that bear scars (rake marks) from killer whale attacks, and to examine the timing of scar acquisition. The results of this study show that there is considerable geographic variation in the proportion of whales with rake marks, ranging from 0% to >40% in different regions. In every region, the great majority of the scars seen were present on the whales’ bodies when the animals were first sighted. Less than 7% (9 of 132) of scarred humpback whales with multi-year sighting histories acquired new scars after the first sighting. This suggests that most killer whale attacks on baleen whales target young animals, probably calves on their first migration from low-latitude breeding and calving areas to high-latitude feeding grounds. Overall, our results imply that adult baleen whales are not an important prey source for killer whales in high latitudes, and therefore that one of the primary assumptions underlying the Springer et al. (2003) prey-switching hypothesis (and its purported link to industrial whaling) is invalid.
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ArticleMultiple steroid and thyroid hormones detected in baleen from eight whale species(Oxford University Press, 2017-11-09) Hunt, Kathleen E. ; Lysiak, Nadine S. J. ; Robbins, Jooke ; Moore, Michael J. ; Seton, Rosemary E. ; Torres, Leigh ; Buck, C. LorenRecent studies have demonstrated that some hormones are present in baleen powder from bowhead (Balaena mysticetus) and North Atlantic right (Eubalaena glacialis) whales. To test the potential generalizability of this technique for studies of stress and reproduction in large whales, we sought to determine whether all major classes of steroid and thyroid hormones are detectable in baleen, and whether these hormones are detectable in other mysticetes. Powdered baleen samples were recovered from single specimens of North Atlantic right, bowhead, blue (Balaenoptera [B.]musculus), sei (B. borealis), minke (B. acutorostrata), fin (B. physalus), humpback (Megaptera novaeangliae) and gray (Eschrichtius robustus) whales. Hormones were extracted with a methanol vortex method, after which we tested all species with commercial enzyme immunoassays (EIAs, Arbor Assays) for progesterone, testosterone, 17β-estradiol, cortisol, corticosterone, aldosterone, thyroxine and tri-iodothyronine, representing a wide array of steroid and thyroid hormones of interest for whale physiology research. In total, 64 parallelism tests (8 species × 8 hormones) were evaluated to verify good binding affinity of the assay antibodies to hormones in baleen. We also tested assay accuracy, although available sample volume limited this test to progesterone, testosterone and cortisol. All tested hormones were detectable in baleen powder of all species, and all assays passed parallelism and accuracy tests. Although only single individuals were tested, the consistent detectability of all hormones in all species indicates that baleen hormone analysis is likely applicable to a broad range of mysticetes, and that the EIA kits tested here perform well with baleen extract. Quantification of hormones in baleen may be a suitable technique with which to explore questions that have historically been difficult to address in large whales, including pregnancy and inter-calving interval, age of sexual maturation, timing and duration of seasonal reproductive cycles, adrenal physiology and metabolic rate.
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ArticleDevelopment and assessment of a new dermal attachment for short-term tagging studies of baleen whales(John Wiley & Sons, 2014-12-18) Baumgartner, Mark F. ; Hammar, Terence R. ; Robbins, JookeCurrent studies of fine-scale baleen whale diving and foraging behaviour rely on archival suction cup tags that remain attached over time scales of hours. However, skin irregularities can make suction cup attachment unreliable, and traditional pole deployment of suction cup tags is challenging in moderate sea conditions or when whales are evasive. We developed a new tag attachment to overcome these limitations. The attachment features a short (6·5–7·5 cm) needle that anchors in the whale's dermis (epidermis and blubber) to which a free-floating tag is attached via a severable tethered link. The needle, tag and a detachable ‘carrier rocket’ with fletching are fitted together to form a projectile that can be deployed at distances of up to 20 m using a compressed-air launcher. A corrosive release mechanism allows the tag to separate from the needle after a specified period of time so that the tag can be recovered. The dermal attachment was evaluated during a study of humpback whales (Megaptera novaeangliae) in the Gulf of Maine and then subsequently deployed on bowhead whales (Balaena mysticetus) near Barrow, Alaska. Monitoring of tagged humpback whales indicated that the needle was shed several days after deployment, the attachment site healed shortly thereafter, and there were no discernible behavioural or health effects over time scales of days to months after tagging. Bowhead whales showed little immediate reaction to tagging; the most common response was a prolonged dive right after tag deployment. On average, respiration rates of tagged bowhead whales were elevated after tag attachment, but returned to the same rate as undisturbed bowheads within 1–1·5 h. When compared to suction cups, the dermal anchor provided a more reliable attachment and it can be applied from greater distances and in rougher sea conditions; it is therefore a useful alternative in circumstances where suction cup tags cannot be easily deployed.
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ArticleHumpback whale populations share a core skin bacterial community : towards a health index for marine mammals?(Public Library of Science, 2014-03-26) Apprill, Amy ; Robbins, Jooke ; Eren, A. Murat ; Pack, Adam A. ; Reveillaud, Julie ; Mattila, David K. ; Moore, Michael J. ; Niemeyer, Misty E. ; Moore, Kathleen M. T. ; Mincer, Tracy J.Microbes are now well regarded for their important role in mammalian health. The microbiology of skin – a unique interface between the host and environment - is a major research focus in human health and skin disorders, but is less explored in other mammals. Here, we report on a cross-population study of the skin-associated bacterial community of humpback whales (Megaptera novaeangliae), and examine the potential for a core bacterial community and its variability with host (endogenous) or geographic/environmental (exogenous) specific factors. Skin biopsies or freshly sloughed skin from 56 individuals were sampled from populations in the North Atlantic, North Pacific and South Pacific oceans and bacteria were characterized using 454 pyrosequencing of SSU rRNA genes. Phylogenetic and statistical analyses revealed the ubiquity and abundance of bacteria belonging to the Flavobacteria genus Tenacibaculum and the Gammaproteobacteria genus Psychrobacter across the whale populations. Scanning electron microscopy of skin indicated that microbial cells colonize the skin surface. Despite the ubiquity of Tenacibaculum and Psychrobater spp., the relative composition of the skin-bacterial community differed significantly by geographic area as well as metabolic state of the animals (feeding versus starving during migration and breeding), suggesting that both exogenous and endogenous factors may play a role in influencing the skin-bacteria. Further, characteristics of the skin bacterial community from these free-swimming individuals were assembled and compared to two entangled and three dead individuals, revealing a decrease in the central or core bacterial community members (Tenacibaculum and Psychrobater spp.), as well as the emergence of potential pathogens in the latter cases. This is the first discovery of a cross-population, shared skin bacterial community. This research suggests that the skin bacteria may be connected to humpback health and immunity and could possibly serve as a useful index for health and skin disorder monitoring of threatened and endangered marine mammals.
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PreprintRebuttal to published article “A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs” by M. Stelfox, J. Hudgins, and M. Sweet( 2016-11) Asmutis-Silvia, Regina ; Barco, Susan G. ; Cole, Tim ; Henry, Allison G. ; Johnson, Amanda ; Knowlton, Amy R. ; Landry, Scott ; Mattila, David K. ; Moore, Michael J. ; Robbins, Jooke ; van der Hoop, JulieWe reviewed the findings of the recently published article by Stelfox et al. (2016): “A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs” published in this journal (Volume 111, pp 6–17) and found that they are both flawed and misleading as they do not accurately reflect the prevalence of “ghost gear” cases reported in the literature. While we commend the authors for recognizing the importance of attempting to quantify the threat and for recommending more comprehensive databases, the methods, results and conclusions of this review have not advanced the understanding of the issue. As authors of the papers on whale entanglements in the North Atlantic that were reviewed by Stelfox et al. (2016) and others who are knowledgeable about the topic, we provide specific comments regarding misrepresentations of both the source of entanglement (e.g., actively fished gear versus “ghost gear”) and the number of reported entanglements for whale species included in the North Atlantic.
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Moving ImageHumpback Whale Seawater Entry Videos(Woods Hole Oceanographic Institution, 2017-07-14) Martins, Maria Clara Iruzun ; Miller, Carolyn ; Hamilton, Philip K. ; Robbins, Jooke ; Zitterbart, Daniel ; Moore, MichaelThese UAS video files show 2 individual humpback whales at the moment where seawater covers and enters the blowholes. Videos here are at half the speed of original UAS videos in order to fully capture the fast moment of seawater entering the blowhole. All videos were taken at Stellwagen Bank under NMFS NOAA Permits 17355, 17355-01 and 21371, and with approval from the Woods Hole Oceanographic Institution Institutional Animal Care and Use Committee.
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ArticleMarine mammal skin microbiotas are influenced by host phylogeny(The Royal Society, 2020-05-20) Apprill, Amy ; Miller, Carolyn A. ; Van Cise, Amy M. ; U'Ren, Jana M. ; Leslie, Matthew S. ; Weber, Laura ; Baird, Robin W. ; Robbins, Jooke ; Landry, Scott ; Bogomolni, Andrea L. ; Waring, Gordon T.Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai‘i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.
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ArticleThe role of sand lances (Ammodytes sp.) in the Northwest Atlantic ecosystem: a synthesis of current knowledge with implications for conservation and management(Wiley, 2020-03-20) Staudinger, Michelle D. ; Goyert, Holly ; Suca, Justin J. ; Coleman, Kaycee ; Welch, Linda ; Llopiz, Joel K. ; Wiley, David N. ; Altman, Irit ; Applegate, Andew ; Auster, Peter J. ; Baumann, Hannes ; Beaty, Julia ; Boelke, Deirdre ; Kaufman, Les ; Loring, Pam ; Moxley, Jerry ; Paton, Suzanne ; Powers, Kevin D. ; Richardson, David E. ; Robbins, Jooke ; Runge, Jeffrey A. ; Smith, Brian ; Spiegel, Caleb ; Steinmetz, HalleyThe American sand lance (Ammodytes americanus, Ammodytidae) and the Northern sand lance (A. dubius, Ammodytidae) are small forage fishes that play an important functional role in the Northwest Atlantic Ocean (NWA). The NWA is a highly dynamic ecosystem currently facing increased risks from climate change, fishing and energy development. We need a better understanding of the biology, population dynamics and ecosystem role of Ammodytes to inform relevant management, climate adaptation and conservation efforts. To meet this need, we synthesized available data on the (a) life history, behaviour and distribution; (b) trophic ecology; (c) threats and vulnerabilities; and (d) ecosystem services role of Ammodytes in the NWA. Overall, 72 regional predators including 45 species of fishes, two squids, 16 seabirds and nine marine mammals were found to consume Ammodytes. Priority research needs identified during this effort include basic information on the patterns and drivers in abundance and distribution of Ammodytes, improved assessments of reproductive biology schedules and investigations of regional sensitivity and resilience to climate change, fishing and habitat disturbance. Food web studies are also needed to evaluate trophic linkages and to assess the consequences of inconsistent zooplankton prey and predator fields on energy flow within the NWA ecosystem. Synthesis results represent the first comprehensive assessment of Ammodytes in the NWA and are intended to inform new research and support regional ecosystem‐based management approaches.
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ArticleAcoustic behavior of humpback whale calves on the feeding ground: Comparisons across age and implications for vocal development(Public Library of Science, 2024-05-29) Zeh, Julia M. ; Adcock, Dana L. ; Perez-Marrufo, Valeria ; Cusano, Dana A. ; Robbins, Jooke ; Tackaberry, Jennifer E. ; Jensen, Frants H. ; Weinrich, Mason T. ; Friedlaender, Ari S. ; Wiley, David N. ; Parks, Susan E.Studying sound production at different developmental stages can provide insight into the processes involved in vocal ontogeny. Humpback whales (Megaptera novaeangliae) are a known vocal learning species, but their vocal development is poorly understood. While studies of humpback whale calves in the early stages of their lives on the breeding grounds and migration routes exist, little is known about the behavior of these immature, dependent animals by the time they reach the feeding grounds. In this study, we used data from groups of North Atlantic humpback whales in the Gulf of Maine in which all members were simultaneously carrying acoustic recording tags attached with suction cups. This allowed for assignment of likely caller identity using the relative received levels of calls across tags. We analyzed data from 3 calves and 13 adults. There were high levels of call rate variation among these individuals and the results represent preliminary descriptions of calf behavior. Our analysis suggests that, in contrast to the breeding grounds or on migration, calves are no longer acoustically cryptic by the time they reach their feeding ground. Calves and adults both produce calls in bouts, but there may be some differences in bout parameters like inter-call intervals and bout durations. Calves were able to produce most of the adult vocal repertoire but used different call types in different proportions. Finally, we found evidence of immature call types in calves, akin to protosyllables used in babbling in other mammals, including humans. Overall, the sound production of humpback whale calves on the feeding grounds appears to be already similar to that of adults, but with differences in line with ontogenetic changes observed in other vocal learning species.