Deep-diving Marine Mammals Research Articles

Relationship between red blood cell lifespan and endogenous carbon monoxide in the common bottlenose dolphin and beluga.

Certain deep-diving marine mammals [i.e., northern elephant seal (Mirounga angustirostris), Weddell seal (Leptonychotes weddellii)] have blood carbon monoxide (CO) levels that are comparable with those of chronic cigarette smokers. Most CO produced in humans is a byproduct of heme degradation, which is released when red blood cells (RBCs) are destroyed. Elevated CO can occur in humans when RBC lifespan decreases. The contribution of RBC turnover to CO concentrations in marine mammals is unknown. Here, we report the first RBC lifespans in two healthy marine mammal species with different diving capacities and heme stores, the shallow-diving bottlenose dolphin (Tursiops truncatus) and deep-diving beluga whale (Delphinapterus leucas), and we relate the lifespans to the levels of CO in blood and breath. The belugas, with high blood heme stores, had the longest mean RBC lifespan compared with humans and bottlenose dolphins. Both cetacean species were found to have three times higher blood CO content compared with humans. The estimated CO production rate from heme degradation indicates some marine mammals may have additional mechanisms for CO production, or delay CO removal from the body, potentially from long-duration breath-holds.NEW & NOTEWORTHY This is the first study to determine the red blood cell lifespan in a marine mammal species. High concentrations of carbon monoxide (CO) were found in the blood of bottlenose dolphins and in the blood and breath of belugas compared with healthy humans. Red blood cell turnover accounted for these high levels in bottlenose dolphins, but there may be alternative mechanisms of endogenous CO production that are contributing to the CO concentrations observed in belugas.

Habitat associations of post-breeding female southern elephant seals (Mirounga leonina) from Península Valdés, Argentina

Research on marine mammal habitat-associations often uses satellite remote sensing of sea surface temperature, chlorophyll concentration, and sea surface height to map mesoscale features, which may indicate areas of enhanced productivity and prey availability. However, for species that feed at depths >400 m, the increased productivity associated with mesoscale features observed near the surface may have little or no immediate effect on habitat-associations at depth. As a result, previous studies have found a weak correlation between mesoscale features and the movements of marine mammals. The advantage of biologging is that hydrographic variables are recorded in situ and at foraging depths using animal-borne instruments with sensors for temperature, conductivity (salinity), and dissolved oxygen. The goal of this study was to characterize the habitat-associations of female southern elephant seals (SES) from Península Valdés, Argentina during the post-breeding foraging trip. Although female SES exhibited significant habitat-associations with sea surface height anomaly and chlorophyll concentrations, the presence or absence of eddies was not predictive of foraging behavior, and the majority of foraging dives (74%) and prey encounters (77%) occurred in the absence of eddies. The strongest habitat-association was with deep (>500 m) and cold (3.73 ± 1.29 °C) subantarctic water, primarily during foraging dives from dusk to dawn. Female SES made most of their foraging dives (68%, mean maximum depth of 539 ± 226 m) and had the most prey encounters (67%) in Antarctic Intermediate Water (AAIW), which is formed near the Subantarctic Front on the northern flank of the Antarctic Circumpolar Current. Our results suggest that AAIW is the principal foraging habitat of female SES from Península Valdés, which may not be directly associated with near-surface mesoscale features. Future research on the habitat-associations for SES and other deep-diving marine mammals should focus on indices of foraging success and the hydrographic features of water masses at foraging depths, not mesoscale features observed near the surface.

First Report of Red Blood Cell Lifespan in a Marine Mammal: An Insight Into Endogenous Carbon Monoxide (CO) Production

Deep-diving marine mammals are known to have high concentrations of hemoglobin (Hb), experience hypoxemia from extended breath-holds, and ischemia-reperfusion events in tissues from the physiological dive response. However, certain deep-diving seals (e.g., elephant and Weddell seals) are known to have levels of carbon monoxide (CO) in their blood that are similar to those seen in chronic cigarette smokers (>10% carboxyhemoglobin; COHb). The source of the high CO in the seals is currently unknown. The gas is naturally produced in humans and lab animals as a byproduct of heme degradation, by heme oxygenase enzymes. Therefore, CO production is tightly correlated with red blood cell (RBC) lifespan and associated Hb degradation, as shown by higher COHb (average 1.9%, maximum 9.7%) in patients with shortened RBC lifespans due to hemolytic anemia. Although normally considered a toxic gas, low levels of CO are naturally produced in most mammals (≤ 1% COHb in healthy humans), and exposure to moderate concentrations of exogenous CO has shown to elicit cytoprotective effects (e.g., anti-inflammation) in tissues exposed to hypoxia or ischemia-reperfusion events. Therefore, there is a desire to ascertain the mechanisms behind the regulation of elevated CO in marine mammals. Similar to humans, the production of high concentrations of CO in marine mammals is hypothesized to be directly related to their RBC lifespan. The RBC lifespan has been determined in a variety of terrestrial vertebrates, but never reported for any marine mammal species. In terrestrial mammals, there is an allometric relationship with larger animals having longer RBC lifespans (RBC lifespan (days) = (body mass (kg)0.132) (68) + 49). This study reports the first measurements of RBC lifespan in a marine mammal, the shallow-diving bottlenose dolphin (mass = 216 ± 23 kg, Hb = 14 g/dl). We hypothesize that the bottlenose dolphin would have a RBC lifespan that is similar to healthy humans (~120 days). Our results show the RBC lifespan of the bottlenose dolphin is 165.7 ± 18.4 days. Like humans, bottlenose dolphins also had low levels of CO in their blood (1.6 ± 0.5 % COHb) and exhaled breath (2.4 ± 1.0 ppm). Ongoing measurements in larger, deeper-diving mammals (e.g., beluga whales, 747 ± 244 kg, Hb = 21 g/dl), will further reveal the impact of heme stores and body mass on RBC lifespan and endogenous CO production in mammals.

Model-based unsupervised clustering for distinguishing Cuvier's and Gervais' beaked whales in acoustic data

Passive acoustic monitoring (PAM), particularly autonomous platforms, offers many advantages in monitoring phonating deep-diving marine mammals in oceanic environment. Relevant data can be obtained day and night continuously over long durations and in any weather conditions. It provides a cost-efficient solution with greater detection ranges when compared to traditional large research vessel and aerial visual surveys requiring keeping expert observers on station for long periods of time and relying on good visibility and calm seas. Therefore, PAM is becoming a preferred tool to assess population dynamics trends and health of deep-water marine mammal stocks. However the large volumes of collected data require robust automatic detection and classification algorithms to identify marine mammals in recordings. As for beaked whales, one of the challenging automatic processing goals is the identification of different species to advance our understanding of their role in the marine ecosystem. At present, traditional detection and classification methods employ searches for acoustic events above a user-defined signal-to-noise ratio threshold in the frequency band of interest and further rely on an experienced operator's manual inspection for species classification and removal of false positives. Current passive monitoring data collection systems yield large volumes of acoustic data, therefore a manual classification approach becomes very time-consuming and impractical. This paper focuses on developing a multi-stage automatic classifier for beaked whale species. The proposed method utilizes unsupervised machine clustering of signal attributes extracted from potential detection events flagged by an energy-band detector. The proposed algorithm was benchmarked against a manually annotated workshop dataset and applied to acoustic data collected in the northern Gulf of Mexico. The algorithm classifies beaked whale species in automatic mode with minimal operator involvement only at the validation stage. When compared with the manually annotated classification dataset, the proposed method achieved a recall rate of 82.8% for Cuvier's and 77.9% for Gervais' species in automatic mode. New insights on habitat use by different species of beaked whales in the Gulf of Mexico were gained when using the species-specific classifier. The high spatial resolution acoustic monitoring results showed that the habitat preferences of two dominating beaked whale species in the Gulf of Mexico support the habitat division (ecological niche) hypothesis.

The Effects of Ship Noise on Marine Mammals—A Review

The number of marine watercraft is on the rise—from private boats in coastal areas to commercial ships crossing oceans. A concomitant increase in underwater noise has been reported in several regions around the globe. Given the important role sound plays in the life functions of marine mammals, research on the potential effects of vessel noise has grown—in particular since the year 2000. We provide an overview of this literature, showing that studies have been patchy in terms of their coverage of species, habitats, vessel types, and types of impact investigated. The documented effects include behavioural and acoustic responses, auditory masking, and stress. We identify knowledge gaps: There appears a bias to more easily accessible species (i.e., bottlenose dolphins and humpback whales), whereas there is a paucity of literature addressing vessel noise impacts on river dolphins, even though some of these species experience chronic noise from boats. Similarly, little is known about the potential effects of ship noise on pelagic and deep-diving marine mammals, even though ship noise is focussed in a downward direction, reaching great depth at little acoustic loss and potentially coupling into sound propagation channels in which sound may transmit over long ranges. We explain the fundamental concepts involved in the generation and propagation of vessel noise and point out common problems with both physics and biology: Recordings of ship noise might be affected by unidentified artefacts, and noise exposure can be both under- and over-estimated by tens of decibel if the local sound propagation conditions are not considered. The lack of anthropogenic (e.g., different vessel types), environmental (e.g., different sea states or presence/absence of prey), and biological (e.g., different demographics) controls is a common problem, as is a lack of understanding what constitutes the ‘normal’ range of behaviours. Last but not least, the biological significance of observed responses is mostly unknown. Moving forward, standards on study design, data analysis, and reporting are badly needed so that results are comparable (across space and time) and so that data can be synthesised to address the grand unknowns: the role of context and the consequences of chronic exposures.

Report of the workshop Evaluating the nature of midwater mining plumes and their potential effects on midwater ecosystems

Report of the workshop Evaluating the nature of midwater mining plumes and their potential effects on midwater ecosystems

Movement and Biosonar Behavior During Prey Encounters Indicate That Male Sperm Whales Switch Foraging Strategy With Depth

Despite their apex predator role, relatively little is known about the foraging strategies that deep-diving marine mammals employ to target prey resources available at different depths with different costs of access. Using hidden Markov model (HMM) analysis of behavioral time series, we aimed to quantify the potential for multiple foraging strategies during 3150 terminal echolocation (‘buzz’) phases of 28 tagged male sperm whales in Northern Norway. Movement metrics included in the HMM reflected the predator’s pursuit path (vertical velocity, pitch and heading variance) and locomotion effort (overall dynamic body acceleration ODBA). We found a highly depth-dependent distribution of four buzz types: “Shallow-sparse” (median 161 m) had the highest inter-buzz intervals, “Mid-active” (372 m) were the longest duration buzzes (median 21 s) and the most active in terms of pitch variance, heading variance and ODBA, while “Deep” and “Deep descent” buzzes (1130-1180 m) were the shortest in duration (~7 s) and least energetic in maneuvers. Regression models for acoustic metrics with both buzz type and depth as explanatory variables revealed that maximum click rate in a buzz had a strong negative linear relationship with ambient pressure (1.2 Hz every 10 atm or 100 m). After accounting for the effects of pressure, buzz click rates were significantly higher during “Mid-active” than other types of buzzes. Within buzzes, apparent click output level (AOL, off-axis level received by the tag, dB re 1 μPa) correlated linearly with log10(inter-click-interval), as expected by acoustic gain control and increasing sensory volume with increasing click rate. These results indicate that while higher acoustic sampling rates were used to track more mobile prey, buzz clicks were produced more sparingly at high ambient pressures where the number of pneumatically produced clicks may be limited before air must be recycled, and where prey seem easier to subdue. The diverse prey base indicated by this study support the feeding requirements of large male sperm whales, and that high feeding rates of more densely distributed and perhaps more predictable resources (e.g. immobile life stages of female Gonatus fabricii) likely maintain preference for the deepest foraging habitats (> 1 km) of this generalist predator.

Marine Mammals' NMDA Receptor Structure: Possible Adaptation to High Pressure Environment.

Divers that are exposed to high pressure (HP) above 1.1 MPa suffer from High Pressure Neurological Syndrome (HPNS), which is implicated with central nervous system (CNS) malfunction. Marine mammals performing extended and deep breath-hold dives are exposed to almost 20 MPa without apparent HPNS symptoms. N-methyl-D-aspartate receptor (NMDAR) has repeatedly been implicated as one of the major factors in CNS hyperexcitability as part of HPNS. Electrophysiological studies in rat brain slices at He HP showed a significant increase in the synaptic NMDAR response, followed by postsynaptic excitability changes. Molecular studies of Rattus norvegicus NMDARs have revealed that different subunit combinations of the NMDAR exhibit different, increased or decreased, current responses under He HP conditions. The purpose of the present research was to disclose if the breath-hold deep diving mammals exhibit NMDAR structural modifications related to HP. We used sequence alignment and homology structure modeling in order to compare deep diving marine mammals’ NMDARs to those of terrestrial mammals. We discovered that deep diving mammals have a special tertiary TMD structure of the GluN2A subunit that differs from that of the terrestrial mammals. In addition, the GluN2A subunit has a group of four conserved a.a. substitutions: V68L (N-terminal domain, NTD) and V440I (agonist-binding domain, ABD) are cetacean specific, E308D (N-terminal domain, NTD) and I816V (transmembrane domain, TMD) were also singularly found in some terrestrial mammals. Since I816V is localized in M4 α-helix region, which is critical for NMDAR activation and desensitization, we hypothesize that the presence of all 4 substitutions rather than a single one, is the combination that may enable HP tolerance. Furthermore, additional special substitutions that were found in the marine mammals’ NTD may affect the Zn2+ binding site, suggesting less or no voltage-independent inhibition by this ion. Our molecular studies of NMDARs containing the GluN2A subunit showed that HP removal of the Zn2+ voltage-independent inhibition could be the mechanism explaining its current increase at HP. Thus, this mechanism could play a crucial role in the CNS hyperexcitability at HP. Less or no voltage-independent Zn2+ inhibition, different conformations of the TMD, and special mutation in the M4 α-helix region of cetaceans’ NMDAR, may give them the advantage they need in order to perform such deep dives without CNS malfunction.

Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance.

Many baleen whales undertake annual fasting and feeding cycles, resulting in substantial changes in their body condition, an important factor affecting fitness. As a measure of lipid-store body condition, tissue density of a few deep diving marine mammals has been estimated using a hydrodynamic glide model of drag and buoyancy forces. Here, we applied the method to shallow-diving humpback whales (Megaptera novaeangliae) in North Atlantic and Antarctic feeding aggregations. High-resolution 3-axis acceleration, depth and speed data were collected from 24 whales. Measured values of acceleration during 5 s glides were fitted to a hydrodynamic glide model to estimate unknown parameters (tissue density, drag term and diving gas volume) in a Bayesian framework. Estimated species-average tissue density (1031.6 ± 2.1 kg m-3, ±95% credible interval) indicates that humpback whale tissue is typically negatively buoyant although there was a large inter-individual variation ranging from 1025.2 to 1043.1 kg m-3. The precision of the individual estimates was substantially finer than the variation across different individual whales, demonstrating a progressive decrease in tissue density throughout the feeding season and comparably high lipid-store in pregnant females. The drag term (CDAm-1) was estimated to be relatively high, indicating a large effect of lift-related induced drag for humpback whales. Our results show that tissue density of shallow diving baleen whales can be estimated using the hydrodynamic gliding model, although cross-validation with other techniques is an essential next step. This method for estimating body condition is likely to be broadly applicable across a range of aquatic animals and environments.

Long-term spatially distributed observations of deep diving marine mammals in the Northern Gulf of Mexico using passive acoustic monitoring

This paper will present the results of processing long-term passive acoustic monitoring (PAM) data collected July through October 2015 in the Northern Gulf of Mexico in the vicinity of the Deep Water Horizon oil spill site to aid in understanding factors driving the distribution of sperm and beaked whales in the Gulf of Mexico. The Littoral Acoustic Demonstration Center -Gulf Ecological Monitoring and Modeling Consortium (LADC-GEMM) deployed five bottom-anchored acoustic moorings (LADC EARS buoys) at 10, 25, and 50 nmi distance from the 2010 oil spill location. Autonomous surface vehicles and a glider were simultaneously operated in the area for the additional collection of PAM data. The daily and monthly activity of three species of beaked whales exhibits spatial and seasonal variability, which appear to be correlated with levels of anthropogenic noise at the monitoring sites. Acoustic detection data are used to estimate abundances at three sites and compare them to the estimates obtained from baseline data collected before (2007) and right after (2010) the oil spill. Long-term abundance trends for both beaked and sperm whales are discussed. [Research supported by GOMRI.]

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals.

Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to >200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in >73% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic 'dive reflex' in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances.

Lung collapse in the diving sea lion: hold the nitrogen and save the oxygen

Lung collapse is considered the primary mechanism that limits nitrogen absorption and decreases the risk of decompression sickness in deep-diving marine mammals. Continuous arterial partial pressure of oxygen profiles in a free-diving female California sea lion (Zalophus californianus) revealed that (i) depth of lung collapse was near 225 m as evidenced by abrupt changes in during descent and ascent, (ii) depth of lung collapse was positively related to maximum dive depth, suggesting that the sea lion increased inhaled air volume in deeper dives and (iii) lung collapse at depth preserved a pulmonary oxygen reservoir that supplemented blood oxygen during ascent so that mean end-of-dive arterial was 74 ± 17 mmHg (greater than 85% haemoglobin saturation). Such information is critical to the understanding and the modelling of both nitrogen and oxygen transport in diving marine mammals.

Using acoustic cue statistics in matrix population models to study short‐term and long‐term marine mammal population dynamics in the northern Gulf of Mexico.

Acoustics is emerging as a viable tool for determining population trends of deep diving marine mammals in addition to conventional transect‐line visual observations which are often limited by weather conditions, short‐time surface presence, costs, etc. In September 2010, following the recent oil spill in the Gulf of Mexico, the Littoral Acoustic Demonstration Center (LADC) conducted a passive acoustic experiment as part of a study of short‐term and long‐term effects of the oil spill on the resident population of marine mammals. Environmental Acoustic Recording System (EARS) buoys were redeployed in three locations: 9 mi, 23 mi, and 50 mi away from the Deepwater Horizon‐oil spill site. LADC previously collected data at these locations in 2001, 2002, 2007. The pre‐spill data are used as a baseline for estimating long‐term population trends. Densities of acoustic phonations of sperm whales, beaked whales, and dolphins are extracted from collected data and used for point estimates of the resident population density. LADC extensive work on an individual acoustic identification is reviewed in the context of mark‐recapture statistics used in matrix population models. Trends in population density after the spill are presented and discussed. [Research is supported by ONR and NSF. Ship services donated by Greenpeace.]

DIFFERENCES IN NICHE BREADTH AMONG SOME TEUTHIVOROUS MESOPELAGIC MARINE MAMMALS

Marine Mammal ScienceVolume 19, Issue 2 p. 400-406 DIFFERENCES IN NICHE BREADTH AMONG SOME TEUTHIVOROUS MESOPELAGIC MARINE MAMMALS Hal Whitehead, Hal Whitehead Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada and Max Planck Institute for Behavioural Physiology, Seewiesen, D-82305 Germany E-mail: [email protected]Search for more papers by this authorColin D. MacLeod, Colin D. MacLeod Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, United Kingdom and Beaked Whale Research Project, Lower Right, 59 Jute Street, Aberdeen AB24 3EX, United KingdomSearch for more papers by this authorPaul Rodhouse, Paul Rodhouse British Antarctic Survey, Natural Environment Research Council, Madingley Road, Cambridge CB3 0ET, United KingdomSearch for more papers by this author Hal Whitehead, Hal Whitehead Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada and Max Planck Institute for Behavioural Physiology, Seewiesen, D-82305 Germany E-mail: [email protected]Search for more papers by this authorColin D. MacLeod, Colin D. MacLeod Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, United Kingdom and Beaked Whale Research Project, Lower Right, 59 Jute Street, Aberdeen AB24 3EX, United KingdomSearch for more papers by this authorPaul Rodhouse, Paul Rodhouse British Antarctic Survey, Natural Environment Research Council, Madingley Road, Cambridge CB3 0ET, United KingdomSearch for more papers by this author First published: 26 August 2006 https://doi.org/10.1111/j.1748-7692.2003.tb01118.xCitations: 29AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Citing Literature Volume19, Issue2April 2003Pages 400-406 RelatedInformation

Hydrostatic-pressure and temperature effects on the molecular order of erythrocyte membranes from deep-, shallow-, and non-diving mammals

Little is known about the cellular mechanisms involved in the tolerance of deep-diving marine mammals to hydrostatic pressures that cause serious pathologies when experienced by other mammals. We compared fatty-acid composition, cholesterol content, and the effects of pressure on the molecular order of erythrocyte membranes from deep-, shallow-, and non-diving mammals to determine how these properties may be related to diving performance. Erythrocytes were collected from two deep-diving phocid pinnipeds (northern elephant seal (Mirounga angustirostris) and harbor seal (Phoca vitulina)), a relatively shallow-diving otariid pinniped (northern fur seal (Callorhinus ursinus)), and several nondiving terrestrial mammals (dog (Canis familiaris), horse (Equus caballus), and cow (Bos taurus)). Fatty-acid composition clearly distinguished the phocids from the other species. The monoene content of erythrocyte membranes was substantially lower (3 vs.»20%), whereas the lipid unsaturation indices, the ratio of α- to γ-linolenic acids, and the proportions of long-chain polyunsaturated fatty acids were substantially higher in the phocids. The cell-membrane cholesterol content was also significantly lower in erythrocytes from the deep-diving phocids (cholesterol:phospholipid ratios 0.2–0.3) than from most other mammals (1.0). Membranes from the phocids were more ordered than those from the shallow- and non-divers, and were also more sensitive to changes in pressure and temperature. The physiological significance of these differences in cell-membrane structure, which affect the order and sensitivity of cell membranes to hydrostatic pressure, is unknown, but they may be important adaptations that allow repeated and prolonged exposure to great hydrostatic pressure.