Browsing by Subject "marine mammal"

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.

Locomotion in any environment requires the use of energy to overcome the physical

forces inherent in the environment. Most large marine vertebrates have evolved

streamlined fusiform body shapes to minimize the resistive force of drag when in

a neutral position, but nearly all behaviors result in some increase in that force.

Too much energy devoted to locomotion may reduce the available surplus necessary

for population-level factors such as reproduction. The population of North Atlantic

right whales has not recovered following legal protection due to decreased fecundity,

including an increase in the intercalf interval, an increase in the years to first calf and

an increase in the number of nulliparous females in the population. This reproductive

impairment appears to be related to deficiencies in storing enough energy to meet the

costs of reproduction. The goal of this study was to determine whether increases in

moving between prey patches at the cost of decreased foraging opportunities could

shift these whales into a situation of negative energy gain. The first step is to

understand the locomotor costs for this species for the key behaviors of traveling and

foraging.

This study investigated the cost of locomotion in right whales by recording the

submerged diving behaviors of free-ranging individuals in both their foraging habitat

in the Bay of Fundy and their calving grounds in the South Atlantic Bight with a

suction-cupped archival tag. The data from the tags were used to quantify the oc-

currence of different behaviors and their associated swimming behaviors and explore

three behavioral strategies that reduce locomotor costs. First, the influence that

changes in blubber thickness has on the buoyancy of these whales was investigated

by comparing the descent and ascent glide durations of individual whales with differ-

ent blubber thicknesses. Next, the depth of surface dives made by animals of different

sizes was related to the depth where additional wave drag is generated. Finally, the

use of intermittent locomotion during foraging was investigated to understand how

much energy is saved by using this gait. The final piece in this study was to deter-

mine the drag related to traveling and foraging behaviors from glides recorded by

the tags and from two different numerical simulations of flow around whales. One, a

custom developed algorithm for multiphase flow, was used to determine the relative

drag, while a second commercial package was used to determine the absolute mag-

nitude of the drag force on the simplest model, the traveling animal. The resulting

drag estimates were then used in a series of theoretical models that estimated the

energetic profit remaining after shifts in the occurrence of traveling and searching

behaviors.

The diving behavior of right whales can be classified into three stereotyped be-

haviors that are characterized by differences in the time spent in different parts of the

water column. The time budgets and swimming movements during these behaviors

matched those in other species, enabling the dive shapes to be classified as foraging,

searching and traveling behaviors. Right whales with thicker blubber layers were

found to perform longer ascent glides and shorter descent glides than those with

thinner blubber layers, consistent with the hypothesis that positive buoyancy does

influence their vertical diving behavior. During horizontal traveling, whales made

shallow dives to depths that were slightly deeper than those that would cause ad-

ditional costs due to wave drag. These dives appear to allow whales to both avoid

the costs of diving as well as the costs of swimming near the surface. Next, whales

were found to glide for 12% of the bottom phases of their foraging dives, and the

use of `stroke-glide' swimming did not prolong foraging duration from that used by

continuous swimmers. Drag coefficients estimated from these glides had an average

of 0.014 during foraging dives and 0.0052 during traveling, values which fall in the

range of those reported for other marine mammals. One numerical simulation deter-

mined drag forces to be comparable, while the other drastically underestimated the

drag of all behaviors. Finally, alterations to the behavioral budgets of these animals

demonstrated their cost of locomotion constitutes a small portion (8-12%) of the

total energy consumed and only extreme increases in traveling time could result in a

negative energy balance. In summary, these results show that locomotor costs are no

more expensive in this species than those of other cetaceans and that when removed

from all the other stressors on this population, these whales are not on an energetic

`knife edge'.