Microplastics in marine mammal blubber, melon, & other tissues: Evidence of translocation.

Marine mammals consume large quantities of microplastic particles, likely via trophic transfer (i.e., through prey who have consumed plastic) and direct consumption from seawater or sediment. Microplastics have been found in the stomachs, gastro-intestinal tracts, and feces of cetaceans and pinnipeds. Translocation of ingested microplastics has been documented in other organs of several aquatic species, but has not been examined in marine mammals. Marine mammals have highly specialized lipid-rich tissues which may increase susceptibility to lipophilic microplastics. Here we demonstrate the occurrence of microplastics, ranging in size, mass concentration, and particle count concentration from 24.4 µm - 1387 µm, 0.59 µg/g - 25.20 µg/g, and 0.04 - 0.39 particles/g, respectively, in four tissues (acoustic fat pad, blubber, lung, & melon) from twelve marine mammal species inclusive of mysticetes, odontocetes, and phocids. Twenty-two individuals were examined for microplastics using a combination of Raman spectroscopy and pyrolysis gas chromatography with mass spectrometry. Overall, 68% of individuals had at least one microplastic particle in at least one of the four tissue types, with the most common polymer and shape observed being polyethylene and fibers, respectively. These findings suggest some proportion of ingested microplastics translocate throughout marine mammal bodies posing an exposure risk to both marine mammals and people. For people, exposure could be directly through consumption for those who rely on marine mammals as food and indirectly to peoples globally who consume the same prey resources as marine mammals. Some individuals examined represent samples obtained over two decades ago, suggesting that this process, and thus exposure risk, has occurred for some time.

Intra-seasonal variation in feeding rates and diel foraging behaviour in a seasonally fasting mammal, the humpback whale.

Antarctic humpback whales forage in summer, coincident with the seasonal abundance of their primary prey, the Antarctic krill. During the feeding season, humpback whales accumulate energy stores sufficient to fuel their fasting period lasting over six months. Previous animal movement modelling work (using area-restricted search as a proxy) suggests a hyperphagic period late in the feeding season, similar in timing to some terrestrial fasting mammals. However, no direct measures of seasonal foraging behaviour existed to corroborate this hypothesis. We attached high-resolution, motion-sensing biologging tags to 69 humpback whales along the Western Antarctic Peninsula throughout the feeding season from January to June to determine how foraging effort changes throughout the season. Our results did not support existing hypotheses: we found a significant reduction in foraging presence and feeding rates from the beginning to the end of the feeding season. During the early summer period, feeding occurred during all hours at high rates. As the season progressed, foraging occurred mostly at night and at lower rates. We provide novel information on seasonal changes in foraging of humpback whales and suggest that these animals, contrary to nearly all other animals that seasonally fast, exhibit high feeding rates soon after exiting the fasting period.

Scaling of maneuvering performance in baleen whales: larger whales outperform expectations.

Despite their enormous size, whales make their living as voracious predators. To catch their much smaller, more maneuverable prey, they have developed several unique locomotor strategies that require high energetic input, high mechanical power output and a surprising degree of agility. To better understand how body size affects maneuverability at the largest scale, we used bio-logging data, aerial photogrammetry and a high-throughput approach to quantify the maneuvering performance of seven species of free-swimming baleen whale. We found that as body size increases, absolute maneuvering performance decreases: larger whales use lower accelerations and perform slower pitch-changes, rolls and turns than smaller species. We also found that baleen whales exhibit positive allometry of maneuvering performance: relative to their body size, larger whales use higher accelerations, and perform faster pitch-changes, rolls and certain types of turns than smaller species. However, not all maneuvers were impacted by body size in the same way, and we found that larger whales behaviorally adjust for their decreased agility by using turns that they can perform more effectively. The positive allometry of maneuvering performance suggests that large whales have compensated for their increased body size by evolving more effective control surfaces and by preferentially selecting maneuvers that play to their strengths.

Risso's dolphins perform spin dives to target deep-dwelling prey.

Foraging decisions of deep-diving cetaceans can provide fundamental insight into food web dynamics of the deep pelagic ocean. Cetacean optimal foraging entails a tight balance between oxygen-conserving dive strategies and access to deep-dwelling prey of sufficient energetic reward. Risso's dolphins (Grampus griseus) displayed a thus far unknown dive strategy, which we termed the spin dive. Dives started with intense stroking and right-sided lateral rotation. This remarkable behaviour resulted in a rapid descent. By tracking the fine-scale foraging behaviour of seven tagged individuals, matched with prey layer recordings, we tested the hypothesis that spin dives are foraging dives targeting deep-dwelling prey. Hunting depth traced the diel movement of the deep scattering layer, a dense aggregation of prey, that resides deep during the day and near-surface at night. Individuals shifted their foraging strategy from deep spin dives to shallow non-spin dives around dusk. Spin dives were significantly faster, steeper and deeper than non-spin dives, effectively minimizing transit time to bountiful mesopelagic prey, and were focused on periods when the migratory prey might be easier to catch. Hence, whereas Risso's dolphins were mostly shallow, nocturnal foragers, their spin dives enabled extended and rewarding diurnal foraging on deep-dwelling prey.

Baleen whale prey consumption based on high-resolution foraging measurements.

Baleen whales influence their ecosystems through immense prey consumption and nutrient recycling1-3. It is difficult to accurately gauge the magnitude of their current or historic ecosystem role without measuring feeding rates and prey consumed. To date, prey consumption of the largest species has been estimated using metabolic models3-9 based on extrapolations that lack empirical validation. Here, we used tags deployed on seven baleen whale (Mysticeti) species (n = 321 tag deployments) in conjunction with acoustic measurements of prey density to calculate prey consumption at daily to annual scales from the Atlantic, Pacific, and Southern Oceans. Our results suggest that previous studies3-9 have underestimated baleen whale prey consumption by threefold or more in some ecosystems. In the Southern Ocean alone, we calculate that pre-whaling populations of mysticetes annually consumed 430 million tonnes of Antarctic krill (Euphausia superba), twice the current estimated total biomass of E. superba10, and more than twice the global catch of marine fisheries today11. Larger whale populations may have supported higher productivity in large marine regions through enhanced nutrient recycling: our findings suggest mysticetes recycled 1.2 × 104 tonnes iron yr-1 in the Southern Ocean before whaling compared to 1.2 × 103 tonnes iron yr-1 recycled by whales today. The recovery of baleen whales and their nutrient recycling services2,3,7 could augment productivity and restore ecosystem function lost during 20th century whaling12,13.

Scaling of heart rate with breathing frequency and body mass in cetaceans.

Plasticity in the cardiac function of a marine mammal facilitates rapid adjustments to the contrasting metabolic demands of breathing at the surface and diving during an extended apnea. By matching their heart rate (fH) to their immediate physiological needs, a marine mammal can improve its metabolic efficiency and maximize the proportion of time spent underwater. Respiratory sinus arrhythmia (RSA) is a known modulation of fH that is driven by respiration and has been suggested to increase cardiorespiratory efficiency. To investigate the presence of RSA in cetaceans and the relationship between fH, breathing rate (fR) and body mass (Mb), we measured simultaneous fH and fR in five cetacean species in human care. We found that a higher fR was associated with a higher mean instantaneous fH (ifH) and minimum ifH of the RSA. By contrast, fH scaled inversely with Mb such that larger animals had lower mean and minimum ifHs of the RSA. There was a significant allometric relationship between maximum ifH of the RSA and Mb, but not fR, which may indicate that this parameter is set by physical laws and not adjusted dynamically with physiological needs. RSA was significantly affected by fR and was greatly reduced with small increases in fR. Ultimately, these data show that surface fHs of cetaceans are complex and the fH patterns we observed are controlled by several factors. We suggest the importance of considering RSA when interpreting fH measurements and particularly how fR may drive fH changes that are important for efficient gas exchange. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins.

BACKGROUND AND OBJECTIVES: Ischemic events, such as ischemic heart disease and stroke, are the number one cause of death globally. Ischemia prevents blood, carrying essential nutrients and oxygen, from reaching tissues, leading to cell and tissue death, and eventual organ failure. While humans are relatively intolerant to ischemic events, other species, such as marine mammals, have evolved a unique tolerance to chronic ischemia/reperfusion during apneic diving. To identify possible molecular features of an increased tolerance for apnea, we examined changes in gene expression in breath-holding dolphins. METHODOLOGY: Here, we capitalized on the adaptations possesed by bottlenose dolphins (Tursiops truncatus) for diving as a comparative model of ischemic stress and hypoxia tolerance to identify molecular features associated with breath holding. Given that signals in the blood may influence physiological changes during diving, we used RNA-Seq and enzyme assays to examine time-dependent changes in gene expression in the blood of breath-holding dolphins. RESULTS: We observed time-dependent upregulation of the arachidonate 5-lipoxygenase (ALOX5) gene and increased lipoxygenase activity during breath holding. ALOX5 has been shown to be activated during hypoxia in rodent models, and its metabolites, leukotrienes, induce vasoconstriction. CONCLUSIONS AND IMPLICATIONS: The upregulation of ALOX5 mRNA occurred within the calculated aerobic dive limit of the species, suggesting that ALOX5 may play a role in the dolphin's physiological response to diving, particularly in a pro-inflammatory response to ischemia and in promoting vasoconstriction. These observations pinpoint a potential molecular mechanism by which dolphins, and perhaps other marine mammals, respond to the prolonged breath holds associated with diving.

Respiratory sinus arrhythmia and submersion bradycardia in bottlenose dolphins (Tursiops truncatus).

Among the many factors that influence the cardiovascular adjustments of marine mammals is the act of respiration at the surface, which facilitates rapid gas exchange and tissue re-perfusion between dives. We measured heart rate (fH) in six adult male bottlenose dolphins (Tursiops truncatus) spontaneously breathing at the surface to quantify the relationship between respiration and fH, and compared this with fH during submerged breath-holds. We found that dolphins exhibit a pronounced respiratory sinus arrhythmia (RSA) during surface breathing, resulting in a rapid increase in fH after a breath followed by a gradual decrease over the following 15-20 s to a steady fH that is maintained until the following breath. RSA resulted in a maximum instantaneous fH (ifH) of 87.4±13.6 beats min-1 and a minimum ifH of 56.8±14.8 beats min-1, and the degree of RSA was positively correlated with the inter-breath interval (IBI). The minimum ifH during 2 min submerged breath-holds where dolphins exhibited submersion bradycardia (36.4±9.0 beats min-1) was lower than the minimum ifH observed during an average IBI; however, during IBIs longer than 30 s, the minimum ifH (38.7±10.6 beats min-1) was not significantly different from that during 2 min breath-holds. These results demonstrate that the fH patterns observed during submerged breath-holds are similar to those resulting from RSA during an extended IBI. Here, we highlight the importance of RSA in influencing fH variability and emphasize the need to understand its relationship to submersion bradycardia.

Exploring movement patterns and changing distributions of baleen whales in the western North Atlantic using a decade of passive acoustic data.

Six baleen whale species are found in the temperate western North Atlantic Ocean, with limited information existing on the distribution and movement patterns for most. There is mounting evidence of distributional shifts in many species, including marine mammals, likely because of climate-driven changes in ocean temperature and circulation. Previous acoustic studies examined the occurrence of minke (Balaenoptera acutorostrata) and North Atlantic right whales (NARW; Eubalaena glacialis). This study assesses the acoustic presence of humpback (Megaptera novaeangliae), sei (B. borealis), fin (B. physalus), and blue whales (B. musculus) over a decade, based on daily detections of their vocalizations. Data collected from 2004 to 2014 on 281 bottom-mounted recorders, totaling 35,033 days, were processed using automated detection software and screened for each species' presence. A published study on NARW acoustics revealed significant changes in occurrence patterns between the periods of 2004-2010 and 2011-2014; therefore, these same time periods were examined here. All four species were present from the Southeast United States to Greenland; humpback whales were also present in the Caribbean. All species occurred throughout all regions in the winter, suggesting that baleen whales are widely distributed during these months. Each of the species showed significant changes in acoustic occurrence after 2010. Similar to NARWs, sei whales had higher acoustic occurrence in mid-Atlantic regions after 2010. Fin, blue, and sei whales were more frequently detected in the northern latitudes of the study area after 2010. Despite this general northward shift, all four species were detected less on the Scotian Shelf area after 2010, matching documented shifts in prey availability in this region. A decade of acoustic observations have shown important distributional changes over the range of baleen whales, mirroring known climatic shifts and identifying new habitats that will require further protection from anthropogenic threats like fixed fishing gear, shipping, and noise pollution.

Acoustic crypsis in communication by North Atlantic right whale mother-calf pairs on the calving grounds.

Mammals with dependent young often rely on cryptic behaviour to avoid detection by potential predators. In the mysticetes, large baleen whales, young calves are known to be vulnerable to direct predation from both shark and orca predators; therefore, it is possible that mother-calf pairs may show cryptic behaviours to avoid the attention of predators. Baleen whales primarily communicate through low-frequency acoustic signals, which can travel over long ranges. In this study, we explore the potential for acoustic crypsis, a form of cryptic behaviour to avoid predator detection, in North Atlantic right whale mother-calf pairs. We predicted that mother-calf pairs would either show reduced calling rates, reduced call amplitude or a combination of these behavioural modifications when compared with other demographic groups in the same habitat. Our results show that right whale mother-calf pairs have a strong shift in repertoire usage, significantly reducing the number of higher amplitude, long-distance communication signals they produced when compared with juvenile and pregnant whales in the same habitat. These observations show that right whale mother-calf pairs rely upon acoustic crypsis, potentially to minimize the risk of acoustic eavesdropping by predators.

North Atlantic right whale (Eubalaena glacialis) acoustic behavior on the calving grounds.

Passive acoustic monitoring is a common method for detection of endangered North Atlantic right whales. This study reports on the acoustic behavior of right whales on the winter calving grounds to assess their acoustic detectability in this habitat. In addition to known call types, previously undescribed low amplitude short broadband signals were detected from lactating females with calves. The production of higher amplitude tonal calls occurred at lower rates for lactating females than from other age/sex classes suggesting that passive acoustic monitoring may be less effective in detecting mother-calf pairs in this critical habitat area.

Soundscape of an Indo-Pacific humpback dolphin (Sousa chinensis) hotspot before windfarm construction in the Pearl River Estuary, China: Do dolphin engage in noise avoidance and passive eavesdropping behavior?

Soundscapes are vital to acoustically specialized animals. Using passive acoustic monitoring data, the temporal and spectral variations in the soundscape of a Chinese white dolphin hotspot were analyzed. By cluster analysis, the 1/3 octave band power spectrum can be grouped into three bands with median overall contribution rates of 35.24, 14.14 and 30.61%. Significant diel and tidal soundscape variations were observed with a generalized linear model. Temporal patterns and frequency ranges of middle frequency band sound matched well with those of fish vocalization, indicating that fish might serve as a signal source. Dolphin sounds were mainly detected in periods involving low levels of ambient sound and without fish vocalization, which could reflect noise avoidance and passive eavesdropping behaviors engaged in by the predator. Pre-construction data can be used to assess the effects of offshore windfarms on acoustic environments and aquatic animals by comparing them with the soundscape of postconstruction and/or postmitigation.

Acoustic Signatures of Left Ventricular Assist Device Thrombosis.

Left ventricular assist devices (LVADs) are life-saving, surgically implanted mechanical heart pumps used to treat patients with advanced heart failure (HF). While life-saving, LVAD support is associated with a high incidence of complications, making early recognition and management of LVAD complications a critical need. Blood clot formation within the LVAD, known as LVAD thrombosis, is a catastrophic complication of LVAD therapy that often requires LVAD exchange due to delayed diagnosis and treatment. Using digital stethoscopes, we identified differences in acoustic spectra from two patients presenting with LVAD thrombosis compared with normally functioning LVAD pumps within the same patient. Importantly, these acoustic changes were present even in the absence of typical signs of HF that are often present in LVAD thrombosis patients. Our work suggests that acoustic spectral analysis of digital stethoscope signals could be used for early detection and mitigation of LVAD complications.

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.

Selective reactions to different killer whale call categories in two delphinid species.

The risk of predation is often invoked as an important factor influencing the evolution of social organization in cetaceans, but little direct information is available about how these aquatic mammals respond to predators or other perceived threats. We used controlled playback experiments to examine the behavioral responses of short-finned pilot whales (Globicephala macrorhynchus) off Cape Hatteras, NC, USA, and Risso's dolphins (Grampus griseus) off the coast of Southern California, USA, to the calls of a potential predator, mammal-eating killer whales. We transmitted calls of mammal-eating killer whales, conspecifics and baleen whales to 10 pilot whales and four Risso's dolphins equipped with multi-sensor archival acoustic recording tags (DTAGs). Only playbacks of killer whale calls resulted in significant changes in tagged animal heading. The strong responses observed in both species occurred only following exposure to a subset of killer whale calls, all of which contained multiple non-linear properties. This finding suggests that these structural features of killer whale calls convey information about predatory risk to pilot whales and Risso's dolphins. The observed responses differed between the two species; pilot whales approached the sound source while Risso's dolphins fled following playbacks. These divergent responses likely reflect differences in anti-predator response mediated by the social structure of the two species.

Diversity of fish sound types in the Pearl River Estuary, China.

BACKGROUND: Repetitive species-specific sound enables the identification of the presence and behavior of soniferous species by acoustic means. Passive acoustic monitoring has been widely applied to monitor the spatial and temporal occurrence and behavior of calling species. METHODS: Underwater biological sounds in the Pearl River Estuary, China, were collected using passive acoustic monitoring, with special attention paid to fish sounds. A total of 1,408 suspected fish calls comprising 18,942 pulses were qualitatively analyzed using a customized acoustic analysis routine. RESULTS: We identified a diversity of 66 types of fish sounds. In addition to single pulse, the sounds tended to have a pulse train structure. The pulses were characterized by an approximate 8 ms duration, with a peak frequency from 500 to 2,600 Hz and a majority of the energy below 4,000 Hz. The median inter-pulsepeak interval (IPPI) of most call types was 9 or 10 ms. Most call types with median IPPIs of 9 ms and 10 ms were observed at times that were exclusive from each other, suggesting that they might be produced by different species. According to the literature, the two section signal types of 1 + 1 and 1 + N10 might belong to big-snout croaker (Johnius macrorhynus), and 1 + N19 might be produced by Belanger's croaker (J. belangerii). DISCUSSION: Categorization of the baseline ambient biological sound is an important first step in mapping the spatial and temporal patterns of soniferous fishes. The next step is the identification of the species producing each sound. The distribution pattern of soniferous fishes will be helpful for the protection and management of local fishery resources and in marine environmental impact assessment. Since the local vulnerable Indo-Pacific humpback dolphin (Sousa chinensis) mainly preys on soniferous fishes, the fine-scale distribution pattern of soniferous fishes can aid in the conservation of this species. Additionally, prey and predator relationships can be observed when a database of species-identified sounds is completed.

Long-term passive acoustic recordings track the changing distribution of North Atlantic right whales (Eubalaena glacialis) from 2004 to 2014.

Given new distribution patterns of the endangered North Atlantic right whale (NARW; Eubalaena glacialis) population in recent years, an improved understanding of spatio-temporal movements are imperative for the conservation of this species. While so far visual data have provided most information on NARW movements, passive acoustic monitoring (PAM) was used in this study in order to better capture year-round NARW presence. This project used PAM data from 2004 to 2014 collected by 19 organizations throughout the western North Atlantic Ocean. Overall, data from 324 recorders (35,600 days) were processed and analyzed using a classification and detection system. Results highlight almost year-round habitat use of the western North Atlantic Ocean, with a decrease in detections in waters off Cape Hatteras, North Carolina in summer and fall. Data collected post 2010 showed an increased NARW presence in the mid-Atlantic region and a simultaneous decrease in the northern Gulf of Maine. In addition, NARWs were widely distributed across most regions throughout winter months. This study demonstrates that a large-scale analysis of PAM data provides significant value to understanding and tracking shifts in large whale movements over long time scales.

Hidden Markov models reveal complexity in the diving behaviour of short-finned pilot whales.

Diving behaviour of short-finned pilot whales is often described by two states; deep foraging and shallow, non-foraging dives. However, this simple classification system ignores much of the variation that occurs during subsurface periods. We used multi-state hidden Markov models (HMM) to characterize states of diving behaviour and the transitions between states in short-finned pilot whales. We used three parameters (number of buzzes, maximum dive depth and duration) measured in 259 dives by digital acoustic recording tags (DTAGs) deployed on 20 individual whales off Cape Hatteras, North Carolina, USA. The HMM identified a four-state model as the best descriptor of diving behaviour. The state-dependent distributions for the diving parameters showed variation between states, indicative of different diving behaviours. Transition probabilities were considerably higher for state persistence than state switching, indicating that dive types occurred in bouts. Our results indicate that subsurface behaviour in short-finned pilot whales is more complex than a simple dichotomy of deep and shallow diving states, and labelling all subsurface behaviour as deep dives or shallow dives discounts a significant amount of important variation. We discuss potential drivers of these patterns, including variation in foraging success, prey availability and selection, bathymetry, physiological constraints and socially mediated behaviour.