Browsing by Author "Nowacek, Douglas"

The ocean environment poses several adversities to usual mammalian function. Perhaps most consequential to life is the lack of air underwater. For marine mammals, like whales and dolphins, that are required to perform breath-hold dives to forage for prey, this necessitates a unique set of adaptations to efficiently manage oxygen resources while diving. In an era of global environmental change, this hostile habitat is expected to become increasingly challenging for air-breathing mammals; warming waters will necessitate deeper foraging trips and noisier oceans may compel unplanned dives to evade perceived threats. An understanding of marine mammals’ solutions to the physiological challenges of a dually-constrained lifestyle is therefore important not only to reveal how marine mammals are built to thrive where other mammals, particularly humans, falter but also the extent to which these adaptations may scale in a changing ocean environment. In this dissertation, I explore the physiological adaptations, particularly those of the cardiovascular and respiratory systems, that this taxon has evolved to mediate the challenges associated with breath-hold diving. I take a multi-scale approach to investigating these physiological traits, exploring hypotheses at the molecular, tissue-specific, and organismal scales. Accordingly, I leverage both familiar and emerging methodologies in the field of marine mammal physiology to examine adaptations that support the extended dive capacities of whales and dolphins. Cellular and molecular responses to environmental stimuli influence tissue-specific and organismal physiological responses. Despite the inextricable link between molecular and organismal physiology, studies of the molecular adaptations of marine mammals for diving are limited, in part due to the logistical complexity of obtaining molecular samples from this difficult-to-study group. To fill this gap, my collaborators and I deployed RNA-seq and enzymatic assays to examine the molecular-level changes that occur in bottlenose dolphins (Tursiops truncatus) performing extended breath-holds (Chapter 1). We demonstrated that dolphins exhibit transcriptomic and proteomic changes that occur in a time-dependent fashion during breath-holding that could support their ability to maintain selective perfusion during diving. The upregulation of ALOX5, a gene targeted for the treatment of eosinophilic asthma in humans, and lipoxygenase suggest a mechanism by which differential gene regulation could contribute to sustained vasoconstriction during the dive response. These findings illustrate the importance of responses at the molecular level for supporting the unique physiology of marine mammals. Coordinated, tissue-specific physiological changes are central to the mammalian dive response. During dives marine mammals drastically reduce their heart rate (fH) while narrowing the blood vessels that supply their peripheral tissues, thereby slowing oxygen consumption of the heart itself as well as reducing the supply of oxygen-rich blood to non-essential tissues. The factors that modulate fH and contribute to diving bradycardia are complex, largely because they are numerous and often linked, but are crucial to understanding oxygen consumption patterns and, ultimately, whole-organism physiology and behavior. Using simultaneous electrocardiographic (ECG) recordings and respirometry, I show that whales and dolphins exhibit a strong cardiorespiratory coupling that may support the conservation of blood oxygen for hypoxia-intolerant tissues during a breath-hold. This variation in fH with breathing, or respiratory sinus arrhythmia (RSA), is modulated by breathing rate (fR) in bottlenose dolphins such that slow breathing results in larger fluctuations in fH (Chapter 2). Following a breath, fH increases rapidly to a maximum and then decreases through the end of the inter-breath interval (IBI). Notably, some of the minimum fH’s of the RSA were comparable to reported diving fH’s for this species suggesting the importance of apnea alone in modulating the fH of a diving marine mammal. I also demonstrate that this cardiorespiratory coupling scales with body size and fR across five cetacean species suggesting both physical scaling laws and dynamic physiological needs play a role in determining the magnitude of the RSA (Chapter 3). These studies highlight the complexity of tissue-specific responses and the need to contextualize physiological rates. Ultimately, it is the interactions of tissues that determine organismal physiology – the fundamental constraint on an organism’s behavior. To investigate the connection between organismal physiology and behavior, I developed a novel method for extracting fR from free-ranging whale biologging tag data (Chapter 4). I found that the high-flow rate and large tidal volume breaths of cetaceans generate movement signals which are captured by the accelerometers of biologging tags, enabling respiration event detection from historical biologging tag datasets. I applied this tool to movement data collected from short-finned pilot whales in Cape Hatteras, North Carolina using digital acoustic recording tags (DTAGs) and examined variation in respiratory patterns associated with diving (Chapter 5). I found that whales vary their pre- and post-dive surface duration and post-dive fR in proportion to the duration and activity of upcoming dives illustrating the physiological challenge of preparing for and recovering from breath-hold diving and highlighting optimization of surface behavior required to support breath-holds. Physiological responses are coordinated across multiple levels of biological organization necessitating the use of various tools and techniques to fully elucidate the adaptations that support marine mammals’ capacity to dive for minutes to hours without a breath. The findings of this dissertation underscore that the physiological function of breath-holding whales and dolphins is coordinated across scales, the physiological responses of cardiovascular and respiratory systems are linked, and sensing vital rates can provide insights into the physiological demands of a dive. Future studies should continue to focus on integrating methods across scales to better understand the physiological function of these animals and its plasticity in a changing ocean.

Animals experience hydrodynamic forces (lift, drag, and side) and moments (pitching, yawing, and rolling) as a result of motion in an aqueous medium. Under selective pressure, most cetaceans, including porpoises, dolphins, and whales, developed a streamlined body shape and modified limbs, which delay the separation of flow, create lower drag when they swim, and therefore decrease their locomotor cost. In order to calculate the locomotor cost and propulsive efficiency of cetaceans, accurate estimates of drag on marine animals are required. However, extra momentum imparted into the fluid from lift and side forces as well as pitching, rolling, and yawing moments (here, the parasitic loads) results in extra drag force on the animal. Therefore, in addition to streaming and delaying flow separation, animals must also minimize excess fluid momentum resulting from parasitic loads. Given the endangered status of the North Atlantic right whale (Eubalaena glacialis; hereafter NARW), analyzing the hydrodynamic characteristics of the NARWs was the focus of this work. Additionally, previous studies showed that body shape of NARWs changes with life stages, reproduction status, nutritive conditions or prey abundance, and the effects of entanglement in fishing gear. Therefore, in this study, computational fluid dynamics (CFD) analysis was performed on multiple 10 m three-dimensional NARW models with different body shapes (e.g., normal condition, emaciated, and pregnant) to measure baseline measurements of flow regimes and hydrodynamic loads on the animal. Swimming speeds covering known right whale speed range (0.125 m/s to 8 m/s) were simulated in most scenarios. In addition to the hydrodynamic effects of different body shapes, drag was also considered a function of parasitic loads. The NARW models were embedded with bone segments that allowed one to manipulate the body pose of the model via adjusting the flippers or the spine of the animal before measuring hydrodynamic drag. By doing so, momentum from parasitic loads was expected to be eliminated. CFD simulations revealed that drag on NARWs is dictated by its irregular outline and that the drag coefficient (0.0071-0.0059; or dimensionless drag) of on NARWs is approximately twice that of many previous estimates for large cetaceans. It was also found that pregnant NARW model encounters the lowest drag coefficient due to delayed flow separation resulting from enlarged abdomen, whereas the emaciated NARW model experiences the highest drag coefficient possibly due to the concavity at the post-nuchal region. These results suggested that drag on NARWs and their thrust power requirements were indeed affected by its body shape but the differences between the three NARW models tested were small. Lastly, minimum drag, which corresponds to the elimination of the parasitic loads, can be obtained by adjusting the pose of the animal. Thus, minimum drag occurs at the neutral trim pose. For the static, normo-nourished NARW model, simulations revealed that by changing the angle of attack of the flippers by 4.03° (relative to the free-stream flow) and pitching the spine downward by 5° while maintaining fluke angle, the drag was lowered by approximately 11% across the flow speeds tested. This drag reduction was relative to the drag study conducted on the same animal model but without body pose adjustments. Together the studies included in the present work explored and highlighted the capability of numerical methods in investigating the hydrodynamics and energetics of cetaceans. Future studies should address how computer solutions can be used to solve problems from a wider aspect. For instance, extra parasitic loads caused by attached gear as well as possible injuries due to the encounter with fishing gear should also be considered while evaluating the energy budget of the North Atlantic right whales.

Social structure is a key determinant of population biology and is central to the way animals exploit their environment. The risk of predation is often invoked as an important factor influencing the evolution of social structure in cetaceans and other mammals, but little direct information is available about how cetaceans actually respond to predators or other perceived threats. The playback of sounds to an animal is a powerful tool for assessing behavioral responses to predators, but quantifying behavioral responses to playback experiments requires baseline knowledge of normal behavioral patterns and variation. The central goal of my dissertation is to describe baseline foraging behavior for the western Atlantic short-finnned pilot whales (Globicephala macrohynchus) and examine the role of social organization in their response to predators. To accomplish this I used multi-sensor digital acoustic tags (DTAGs), satellite-linked time-depth recorders (SLTDR), and playback experiments to study foraging behavior and behavioral response to predators in pilot whales. Fine scale foraging strategies and population level patterns were identified by estimating the body size and examining the location and movement around feeding events using data collected with DTAGs deployed on 40 pilot whales in summers of 2008-2014 off the coast of Cape Hatteras, North Carolina. Pilot whales were found to forage throughout the water column and performed feeding buzzes at depths ranging from 29-1176 meters. The results indicated potential habitat segregation in foraging depth in short-finned pilot whales with larger individuals foraging on average at deeper depths. Calculated aerobic dive limit for large adult males was approximately 6 minutes longer than that of females and likely facilitated the difference in foraging depth. Furthermore, the buzz frequency and speed around feeding attempts indicate this population pilot whales are likely targeting multiple small prey items. Using these results, I built decision trees to inform foraging dive classification in coarse, long-term dive data collected with SLTDRs deployed on 6 pilot whales in the summers of 2014 and 2015 in the same area off the coast of North Carolina. I used these long term foraging records to compare diurnal foraging rates and depths, as well as classify bouts with a maximum likelihood method, and evaluate behavioral aerobic dive limits (ADLB) through examination of dive durations and inter-dive intervals. Dive duration was the best predictor of foraging, with dives >400.6 seconds classified as foraging, and a 96% classification accuracy. There were no diurnal patterns in foraging depth or rates and average duration of bouts was 2.94 hours with maximum bout durations lasting up to 14 hours. The results indicated that pilot whales forage in relatively long bouts and the ADLB indicate that pilot whales rarely, if ever exceed their aerobic limits. To evaluate the response to predators I used controlled playback experiments to examine the behavioral responses of 10 of the tagged short-finned pilot whales off Cape Hatteras, North Carolina and 4 Risso’s dolphins (Grampus griseus) off Southern California to the calls of mammal-eating killer whales (MEK). Both species responded to a subset of MEK calls with increased movement, swim speed and increased cohesion of the focal groups, but the two species exhibited different directional movement and vocal responses. Pilot whales increased their call rate and approached the sound source, but Risso’s dolphins exhibited no change in their vocal behavior and moved in a rapid, directed manner away from the source. Thus, at least to a sub-set of mammal-eating killer whale calls, these two study species reacted in a manner that is consistent with their patterns of social organization. Pilot whales, which live in relatively permanent groups bound by strong social bonds, responded in a manner that built on their high levels of social cohesion. In contrast, Risso’s dolphins exhibited an exaggerated flight response and moved rapidly away from the sound source. The fact that both species responded strongly to a select number of MEK calls, suggests that structural features of signals play critical contextual roles in the probability of response to potential threats in odontocete cetaceans.

This dissertation focuses on two vital challenges in relation to whale acoustic signals: detection and classification.

In detection, we evaluated the influence of the uncertain ocean environment on the spectrogram-based detector, and derived the likelihood ratio of the proposed Short Time Fourier Transform detector. Experimental results showed that the proposed detector outperforms detectors based on the spectrogram. The proposed detector is more sensitive to environmental changes because it includes phase information.

In classification, our focus is on finding a robust and sparse representation of whale vocalizations. Because whale vocalizations can be modeled as polynomial phase signals, we can represent the whale calls by their polynomial phase coefficients. In this dissertation, we used the Weyl transform to capture chirp rate information, and used a two dimensional feature set to represent whale vocalizations globally. Experimental results showed that our Weyl feature set outperforms chirplet coefficients and MFCC (Mel Frequency Cepstral Coefficients) when applied to our collected data.

Since whale vocalizations can be represented by polynomial phase coefficients, it is plausible that the signals lie on a manifold parameterized by these coefficients. We also studied the intrinsic structure of high dimensional whale data by exploiting its geometry. Experimental results showed that nonlinear mappings such as Laplacian Eigenmap and ISOMAP outperform linear mappings such as PCA and MDS, suggesting that the whale acoustic data is nonlinear.

We also explored deep learning algorithms on whale acoustic data. We built each layer as convolutions with either a PCA filter bank (PCANet) or a DCT filter bank (DCTNet). With the DCT filter bank, each layer has different a time-frequency scale representation, and from this, one can extract different physical information. Experimental results showed that our PCANet and DCTNet achieve high classification rate on the whale vocalization data set. The word error rate of the DCTNet feature is similar to the MFSC in speech recognition tasks, suggesting that the convolutional network is able to reveal acoustic content of speech signals.

Beaked whales (family Ziphiidae) and sperm whales (Physeter macrocephalus) are apex marine predators found throughout the world’s deep oceans. These species are challenging to observe, and little is known about fundamental aspects of their ecology, including their spatiotemporal distributions and habitat use. Passive acoustic monitoring (PAM), can be used to detect their echolocation clicks during foraging dives, thereby providing an indication of species presence. My dissertation investigates the distribution, seasonal occurrence, and diel variability in acoustic detections of beaked whales and sperm whales in the western North Atlantic Ocean, using multi-year passive acoustic recordings collected along the continental slope between Florida and Nova Scotia. First, I describe spatiotemporal patterns in detections of beaked whale echolocation clicks from five beaked whale species and one signal type of unknown origin. At least two beaked whale click types were detected at each recording site, and detections occurred year-round, with site-specific variation in relative species occurrence. Notably, Cuvier’s beaked whales (Ziphius cavirostris) were regularly detected in a region where they have not been commonly observed, and potential habitat partitioning among Cuvier’s and Gervais’ (Mesoplodon europaeus) beaked whales was apparent within their overlapping ranges. To examine the potential effects of using duty-cycled recording schedules on the detection of beaked whale clicks, I performed a subsampling experiment, and found that short, frequent listening periods were most effective for assessing daily presence of beaked whales. Furthermore, subsampling at low duty cycles led to consistently greater underestimation of Mesoplodon species than either Cuvier’s beaked whales or northern bottlenose whales (Hyperoodon ampullatus), leading to a potential bias in estimation of relative species occurrence. Next, I examine the occurrence of sperm whale echolocation clicks, which were recorded commonly between southern New England and North Carolina, but infrequently off the coast of Florida. In the northern half of the study region, I observed distinct seasonal patterns in the daily prevalence of sperm whale clicks, with a winter peak in occurrence off Cape Hatteras, North Carolina, followed by an increase later in the spring at sites further north, suggesting a shift in sperm whale concentrations which may relate to enhanced productivity occurring at higher latitudes in the spring. Finally, I explore the variability in daily detection rates of beaked whales and sperm whales in relation to dynamic oceanographic conditions off the Mid-Atlantic coast. Detection rates did not appear to correlate with temporal environmental variability, and persistent habitat features may be more important in predicting the occurrence of these species. Together, my dissertation provides substantial baseline information on the spatiotemporal occurrence of beaked and sperm whales in the western North Atlantic Ocean, highlighting the diversity within this guild of deep-diving odontocetes and demonstrating the use of PAM to provide species-specific insight into their ecology.

In this work, I explore the impacts of anthropogenic climate change on the krill-reliant marine ecosystem of the western Antarctic Peninsula. I use long-term ecological monitoring data to examine the impact of highly variable krill recruitment on a krill predator population, and I use archived backscatter data from an Acoustic Doppler Current Profiler (ADCP) to investigate biotic and abiotic drivers of summer krill distribution along the mid-to-coastal shelf region of the western Antarctic Peninsula.In Chapter 1, my coauthors and I examine the impact of cyclical krill recruitment on Adélie penguins. Between 1992 and 2018, the breeding population of Adélie penguins around Anvers Island, Antarctica declined by 98%. In this region, natural climate variability drives five-year cycling in marine phytoplankton productivity, leading to phase-offset five-year cycling in the size of the krill population. We demonstrate that the rate of change of the Adélie breeding population also shows five-year cycling. We link this population response to cyclical krill scarcity, a phenomenon which appears to have arisen from the interaction between climate variability and climate change trends. Modeling suggests that, since at least 1980, natural climate variability has driven cycling in this marine system. However, anthropogenic climate change has shifted conditions so that fewer years in each cycle now prompt strong krill recruitment, triggering intervals of krill scarcity that result in drastic declines in Adélie penguins. Our results imply that climate change can amplify the impacts of natural climate oscillations across trophic levels, driving cycling across species and disrupting food webs. The findings indicate that climate variability plays an integral role in driving ecosystem dynamics under climate change. In Chapter 2, I explore the viability of using archived Acoustic Doppler Current Profiler (ADCP) backscatter data to examine krill distribution on the WAP. During the Palmer LTER’s oceanographic cruises, the ship runs an ADCP the entire time it is at sea. An ADCP is a sonar instrument designed to measure water velocity across the water column, but the collected data can also be repurposed to provide information on the distribution and density of sound-scattering objects. Therefore, in regions where the primary sound-scattering objects are zooplankton, the ADCP can be used to map zooplankton distribution. I explore whether archived data (2005-2018) from an ADCP on Palmer LTER sampling cruises can be retroactively analyzed to provide information about the amount and distribution of krill in the water column along the western Antarctic Peninsula. I found that, given the uncertainty on several key instrument parameters, the ADCP’s estimates of krill biovolume are likely to have uncertainty spanning at least an order of magnitude and therefore the ADCP cannot on its own be used to estimate absolute biovolume. However, available evidence suggested that variability in seawater properties and ADCP system parameters is either low and/or can be accounted for using available measurements, and therefore meaningful relative biovolume estimates can theoretically be achieved. Several challenges – including the mismatch between depths sampled by the ADCP and those sampled by net tows, as well as the fact that krill are not the only species present in the sampled region – add uncertainty to comparisons between ADCP data and ground-truthing data available from tows. However, I found highly significant though noisy empirical relationships between the biovolume of krill in tows and the backscatter coefficient calculated from the ADCP, indicating that the ADCP does give useful information about the amount of krill and can be used to map krill distribution along the ship track. In Chapter 3, I use the ADCP backscatter data from Palmer LTER cruises to explore the effect of abiotic and biotic factors on krill distribution along the mid-to-coastal shelf region of the WAP. I find that krill recruitment around Palmer Station is more closely linked to krill density 600km south than to krill density on the sampling line next to Palmer Station, suggesting that krill density further south along the Peninsula is more dependent on recent recruitment than krill density further north. Net tows support this idea, indicating that a larger proportion of recruits are found in the south of the grid than in the north. I also determine that the distance between patches of high biomass becomes exponentially greater with increasing time since a high krill recruitment event, indicating that the foraging conditions become much more difficult as time elapses since a high krill recruitment event. I find evidence that krill are spatially correlated with areas of high primary productivity, suggesting that krill may move to aggregate in these areas and that changing distributions of primary productivity under climate change are likely to change krill distributions. I examine whether krill show avoidance behaviors, such as retreating to colder water at depth, in response to high summer temperatures, but I find no evidence of this and even find a spatial correlation between krill and areas of higher temperature. I conclude that krill are likely not yet temperature-stressed in this region of the WAP. Overall, lowered primary productivity and krill recruitment – and perhaps temperature as it becomes even warmer – will likely have major impacts on the distribution of krill, and therefore on their accessibility to predators and fisheries.