Dynamic body acceleration as a proxy to predict the cost of locomotion in bottlenose dolphins.

Estimates of the energetic costs of locomotion (COL) at different activity levels are necessary to answer fundamental eco-physiological questions and to understand the impacts of anthropogenic disturbance to marine mammals. We combined estimates of energetic costs derived from breath-by-breath respirometry with measurements of overall dynamic body acceleration (ODBA) from biologging tags to validate ODBA as a proxy for COL in trained common bottlenose dolphins (Tursiops truncatus). We measured resting metabolic rate (RMR); mean individual RMR was 0.71-1.42 times that of a similarly sized terrestrial mammal and agreed with past measurements that used breath-by-breath and flow-through respirometry. We also measured energy expenditure during submerged swim trials, at primarily moderate exercise levels. We subtracted RMR to obtain COL, and normalized COL by body size to incorporate individual swimming efficiencies. We found both mass-specific energy expenditure and mass-specific COL were linearly related with ODBA. Measurements of activity level and cost of transport (the energy required to move a given distance) improve understanding of the COL in marine mammals. The strength of the correlation between ODBA and COL varied among individuals, but the overall relationship can be used at a broad scale to estimate the energetic costs of disturbance and daily locomotion costs to build energy budgets, and investigate the costs of diving in free-ranging animals where bio-logging data are available. We propose that a similar approach could be applied to other cetacean species.

Tag-based estimates of bottlenose dolphin swimming behavior and energetics.

Current estimates of marine mammal hydrodynamic forces tend to be made using camera-based kinematic data for a limited number of fluke strokes during a prescribed swimming task. In contrast, biologging tag data yield kinematic measurements from thousands of strokes, enabling new insights into swimming behavior and mechanics. However, there have been limited tag-based estimates of mechanical work and power. In this work, we investigated bottlenose dolphin (Tursiops truncatus) swimming behavior using tag-measured kinematics and a hydrodynamic model to estimate propulsive power, work and cost of transport. Movement data were collected from six animals during prescribed straight-line swimming trials to investigate swimming mechanics over a range of sustained speeds (1.9-6.1 m s-1). Propulsive power ranged from 66 W to 3.8 kW over 282 total trials. During the lap trials, the dolphins swam at depths that mitigated wave drag, reducing overall drag throughout these mid- to high-speed tasks. Data were also collected from four individuals during undirected daytime (08:30-18:00 h) swimming to examine how self-selected movement strategies are used to modulate energetic efficiency and effort. Overall, self-selected swimming speeds (individual means ranging from 1.0 to 1.96 m s-1) tended to minimize cost of transport, and were on the lower range of animal-preferred speeds reported in literature. The results indicate that these dolphins moderate propulsive effort and efficiency through a combination of speed and depth regulation. This work provides new insights into dolphin swimming behavior in both prescribed tasks and self-selected swimming, and presents a path forward for continuous estimates of mechanical work and power from wild animals.

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.

RESPIRATORY CHANGES IN STRANDED BOTTLENOSE DOLPHINS (TURSIOPS TRUNCATUS).

Lung function (breath duration, respiratory flow [V̇], and tidal volume [VT]), and end-expiratory O2 were measured in 19 adult bottlenose dolphins (Tursiops spp.) while at rest in water or beached for up to 10 min. The results show that inspiratory VT, expiratory VT, or inspiratory V̇ did not differ on land or in water. The average expiratory V̇ for all dolphins on land decreased by 16%, and the expiratory and total breath durations increased by 5% and 4%, respectively, compared with in water. There were temporal changes observed during beaching, where expired and inspired VT and inspired V̇ decreased by 13%, 16%, and 9%, respectively, after 10 min on land. These data suggest that dolphins compensate for the effect of gravity by adjusting respiration to maintain alveolar ventilation and gas exchange, but during extended durations, the increased work of breathing may impede ventilation and gas exchange. Continuous monitoring of lung function and gas exchange may help prevent long-term damage during out-of-water medical procedures, optimize animal transport conditions, and improve survival during stranding events.

Cardiorespiratory coupling in cetaceans; a physiological strategy to improve gas exchange?

In the current study we used transthoracic echocardiography to measure stroke volume (SV), heart rate (fH) and cardiac output (CO) in adult bottlenose dolphins (Tursiops truncatus), a male beluga whale calf [Delphinapterus leucas, body mass (Mb) range: 151-175 kg] and an adult female false killer whale (Pseudorca crassidens, estimated Mb: 500-550 kg) housed in managed care. We also recorded continuous electrocardiogram (ECG) in the beluga whale, bottlenose dolphin, false killer whale, killer whale (Orcinus orca) and pilot whale (Globicephala macrorhynchus) to evaluate cardiorespiratory coupling while breathing spontaneously under voluntary control. The results show that cetaceans have a strong respiratory sinus arrythmia (RSA), during which both fH and SV vary within the interbreath interval, making average values dependent on the breathing frequency (fR). The RSA-corrected fH was lower for all cetaceans compared with that of similarly sized terrestrial mammals breathing continuously. As compared with terrestrial mammals, the RSA-corrected SV and CO were either lower or the same for the dolphin and false killer whale, while both were elevated in the beluga whale. When plotting fR against fH for an inactive mammal, cetaceans had a greater cardiac response to changes in fR as compared with terrestrial mammals. We propose that these data indicate an important coupling between respiration and cardiac function that enhances gas exchange, and that this RSA is important to maximize gas exchange during surface intervals, similar to that reported in the elephant seal.

Ventilation and gas exchange before and after voluntary static surface breath-holds in clinically healthy bottlenose dolphins, Tursiops truncatus.

We measured respiratory flow (V̇), breathing frequency (fR), tidal volume (VT), breath duration and end-expired O2 content in bottlenose dolphins (Tursiops truncatus) before and after static surface breath-holds ranging from 34 to 292 s. There was considerable variation in the end-expired O2, VT and fR following a breath-hold. The analysis suggests that the dolphins attempt to minimize recovery following a dive by altering VT and fR to rapidly replenish the O2 stores. For the first breath following a surface breath-hold, the end-expired O2 decreased with dive duration, while VT and fR increased. Throughout the recovery period, end-expired O2 increased while the respiratory effort (VT, fR) decreased. We propose that the dolphins alter respiratory effort following a breath-hold according to the reduction in end-expired O2 levels, allowing almost complete recovery after 1.2 min.

Lung mechanics and pulmonary function testing in cetaceans.

We measured esophageal pressures, respiratory flow rates, and expired O2 and CO2 in six adult bottlenose dolphins (Tursiops truncatus) during voluntary breaths and maximal (chuff) respiratory efforts. The data were used to estimate the dynamic specific lung compliance (sCL), the O2 consumption rate (V̇O2 ) and CO2 production rates (V̇CO2 ) during rest. Our results indicate that bottlenose dolphins have the capacity to generate respiratory flow rates that exceed 130 l s(-1) and 30 l s(-1) during expiration and inspiration, respectively. The esophageal pressures indicated that expiration is passive during voluntary breaths, but active during maximal efforts, whereas inspiration is active for all breaths. The average sCL of dolphins was 0.31±0.04 cmH2O(-1), which is considerably higher than that of humans (0.08 cmH2O(-1)) and that previously measured in a pilot whale (0.13 cmH2O(-1)). The average estimated V̇O2  and V̇CO2  using our breath-by-breath respirometry system ranged from 0.857 to 1.185 l O2 min(-1) and 0.589 to 0.851 l CO2 min(-1), respectively, which is similar to previously published metabolic measurements from the same animals using conventional flow-through respirometry. In addition, our custom-made system allows us to approximate end tidal gas composition. Our measurements provide novel data for respiratory physiology in cetaceans, which may be important for clinical medicine and conservation efforts.

Bottlenose dolphins modify behavior to reduce metabolic effect of tag attachment.

Attaching bio-telemetry or -logging devices ('tags') to marine animals for research and monitoring adds drag to streamlined bodies, thus affecting posture, swimming gaits and energy balance. These costs have never been measured in free-swimming cetaceans. To examine the effect of drag from a tag on metabolic rate, cost of transport and swimming behavior, four captive male dolphins (Tursiops truncatus) were trained to swim a set course, either non-tagged (n=7) or fitted with a tag (DTAG2; n=12), and surface exclusively in a flow-through respirometer in which oxygen consumption VO2 and carbon dioxide production (VO2; ml kg(-1) min(-1)) rates were measured and respiratory exchange ratio (VO2/resting VO2) was calculated. Tags did not significantly affect individual mass-specific oxygen consumption, physical activity ratios (exercise /resting ), total or net cost of transport (COT; J m(-1) kg(-1)) or locomotor costs during swimming or two-minute recovery phases. However, individuals swam significantly slower when tagged (by ~11%; mean ± s.d., 3.31±0.35 m s(-1)) than when non-tagged (3.73±0.41 m s(-1)). A combined theoretical and computational fluid dynamics model estimating drag forces and power exertion during swimming suggests that drag loading and energy consumption are reduced at lower swimming speeds. Bottlenose dolphins in the specific swimming task in this experiment slowed to the point where the tag yielded no increases in drag or power, while showing no difference in metabolic parameters when instrumented with a DTAG2. These results, and our observations, suggest that animals modify their behavior to maintain metabolic output and energy expenditure when faced with tag-induced drag.

Quantifying the age structure of free-ranging delphinid populations: Testing the accuracy of Unoccupied Aerial System photogrammetry.

Understanding the population health status of long-lived and slow-reproducing species is critical for their management. However, it can take decades with traditional monitoring techniques to detect population-level changes in demographic parameters. Early detection of the effects of environmental and anthropogenic stressors on vital rates would aid in forecasting changes in population dynamics and therefore inform management efforts. Changes in vital rates strongly correlate with deviations in population growth, highlighting the need for novel approaches that can provide early warning signs of population decline (e.g., changes in age structure). We tested a novel and frequentist approach, using Unoccupied Aerial System (UAS) photogrammetry, to assess the population age structure of small delphinids. First, we measured the precision and accuracy of UAS photogrammetry in estimating total body length (TL) of trained bottlenose dolphins (Tursiops truncatus). Using a log-transformed linear model, we estimated TL using the blowhole to dorsal fin distance (BHDF) for surfacing animals. To test the performance of UAS photogrammetry to age-classify individuals, we then used length measurements from a 35-year dataset from a free-ranging bottlenose dolphin community to simulate UAS estimates of BHDF and TL. We tested five age classifiers and determined where young individuals (<10 years) were assigned when misclassified. Finally, we tested whether UAS-simulated BHDF only or the associated TL estimates provided better classifications. TL of surfacing dolphins was overestimated by 3.3% ±3.1% based on UAS-estimated BHDF. Our age classifiers performed best in predicting age-class when using broader and fewer (two and three) age-class bins with ~80% and ~72% assignment performance, respectively. Overall, 72.5%-93% of the individuals were correctly classified within 2 years of their actual age-class bin. Similar classification performances were obtained using both proxies. UAS photogrammetry is a non-invasive, inexpensive, and effective method to estimate TL and age-class of free-swimming dolphins. UAS photogrammetry can facilitate the detection of early signs of population changes, which can provide important insights for timely management decisions.

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)'.

Comparative Respiratory Physiology in Cetaceans.

In the current study, we used breath-by-breath respirometry to evaluate respiratory physiology under voluntary control in a male beluga calf [Delphinapterus leucas, body mass range (M b): 151-175 kg], an adult female (estimated M b = 500-550 kg) and a juvenile male (M b = 279 kg) false killer whale (Pseudorca crassidens) housed in managed care. Our results suggest that the measured breathing frequency (f R) is lower, while tidal volume (V T) is significantly greater as compared with allometric predictions from terrestrial mammals. Including previously published data from adult bottlenose dolphin (Tursiops truncatus) beluga, harbor porpoise (Phocoena phocoena), killer whale (Orcinus orca), pilot whale (Globicephala scammoni), and gray whale (Eschrichtius robustus) show that the allometric mass-exponents for V T and f R are similar to that for terrestrial mammals (V T: 1.00, f R: -0.20). In addition, our results suggest an allometric relationship for respiratory flow ( V . ), with a mass-exponent between 0.63 and 0.70, and where the expiratory V . was an average 30% higher as compared with inspiratory V . . These data provide enhanced understanding of the respiratory physiology of cetaceans and are useful to provide proxies of lung function to better understand lung health or physiological limitations.

Using Respiratory Sinus Arrhythmia to Estimate Inspired Tidal Volume in the Bottlenose Dolphin (Tursiops truncatus).

Man-made environmental change may have significant impact on apex predators, like marine mammals. Thus, it is important to assess the physiological boundaries for survival in these species, and assess how climate change may affect foraging efficiency and the limits for survival. In the current study, we investigated whether the respiratory sinus arrhythmia (RSA) could estimate tidal volume (V T) in resting bottlenose dolphins (Tursiops truncatus). For this purpose, we measured respiratory flow and electrocardiogram (ECG) in five adult bottlenose dolphins at rest while breathing voluntarily. Initially, an exponential decay function, using three parameters (baseline heart rate, the change in heart rate following a breath, and an exponential decay constant) was used to describe the temporal change in instantaneous heart rate following a breath. The three descriptors, in addition to body mass, were used to develop a Generalized Additive Model (GAM) to predict the inspired tidal volume (V Tinsp). The GAM allowed us to predict V Tinsp with an average ( ± SD) overestimate of 3 ± 2%. A jackknife sensitivity analysis, where 4 of the five dolphins were used to fit the GAM and the 5th dolphin used to make predictions resulted in an average overestimate of 2 ± 10%. Future studies should be used to assess whether similar relationships exist in active animals, allowing V T to be studied in free-ranging animals provided that heart rate can be measured.