Fast and Furious: Energetic Tradeoffs and Scaling of High-Speed Foraging in Rorqual Whales
INTEGRATIVE ORGANISMAL BIOLOGY
2022; 4 (1): obac038
Although gigantic body size and obligate filter feeding mechanisms have evolved in multiple vertebrate lineages (mammals and fishes), intermittent ram (lunge) filter feeding is unique to a specific family of baleen whales: rorquals. Lunge feeding is a high cost, high benefit feeding mechanism that requires the integration of unsteady locomotion (i.e., accelerations and maneuvers); the impact of scale on the biomechanics and energetics of this foraging mode continues to be the subject of intense study. The goal of our investigation was to use a combination of multi-sensor tags paired with UAS footage to determine the impact of morphometrics such as body size on kinematic lunging parameters such as fluking timing, maximum lunging speed, and deceleration during the engulfment period for a range of species from minke to blue whales. Our results show that, in the case of krill-feeding lunges and regardless of size, animals exhibit a skewed gradient between powered and fully unpowered engulfment, with fluking generally ending at the point of both the maximum lunging speed and mouth opening. In all cases, the small amounts of propulsive thrust generated by the tail were unable to overcome the high drag forces experienced during engulfment. Assuming this thrust to be minimal, we predicted the minimum speed of lunging across scale. To minimize the energetic cost of lunge feeding, hydrodynamic theory predicts slower lunge feeding speeds regardless of body size, with a lower boundary set by the ability of the prey to avoid capture. We used empirical data to test this theory and instead found that maximum foraging speeds remain constant and high (∼4 m s-1) across body size, even as higher speeds result in lower foraging efficiency. Regardless, we found an increasing relationship between body size and this foraging efficiency, estimated as the ratio of energetic gain from prey to energetic cost. This trend held across timescales ranging from a single lunge to a single day and suggests that larger whales are capturing more prey-and more energy-at a lower cost.
View details for DOI 10.1093/iob/obac038
View details for Web of Science ID 000855481000001
View details for PubMedID 36127894
View details for PubMedCentralID PMC9475666
Blue whales increase feeding rates at fine-scale ocean features.
Proceedings. Biological sciences
2022; 289 (1981): 20221180
Marine predators face the challenge of reliably finding prey that is patchily distributed in space and time. Predators make movement decisions at multiple spatial and temporal scales, yet we have a limited understanding of how habitat selection at multiple scales translates into foraging performance. In the ocean, there is mounting evidence that submesoscale (i.e. less than 100 km) processes drive the formation of dense prey patches that should hypothetically provide feeding hot spots and increase predator foraging success. Here, we integrated environmental remote-sensing with high-resolution animal-borne biologging data to evaluate submesoscale surface current features in relation to the habitat selection and foraging performance of blue whales in the California Current System. Our study revealed a consistent functional relationship in which blue whales disproportionately foraged within dynamic aggregative submesoscale features at both the regional and feeding site scales across seasons, regions and years. Moreover, we found that blue whale feeding rates increased in areas with stronger aggregative features, suggesting that these features indicate areas of higher prey density. The use of fine-scale, dynamic features by foraging blue whales underscores the need to take these features into account when designating critical habitat and may help inform strategies to mitigate the impacts of human activities for the species.
View details for DOI 10.1098/rspb.2022.1180
View details for PubMedID 35975432
An accelerometer-derived ballistocardiogram method for detecting heartrates in free-ranging marine mammals.
The Journal of experimental biology
Physio-logging methods, which use animal-borne devices to record physiological variables, are entering a new era driven by advances in sensor development. However, existing datasets collected with traditional bio-loggers, such as accelerometers, still contain untapped eco-physiological information. Here we present a computational method for extracting heartrate from high-resolution accelerometer data using a ballistocardiogram. We validated our method with simultaneous accelerometer-electrocardiogram tag deployments in a controlled setting on a killer whale (Orcinus orca) and demonstrate the predictions correspond with previously observed cardiovascular patterns in a blue whale (Balaenoptera musculus), including the magnitude of apneic bradycardia and increase in heart rate prior to and during ascent. Our ballistocardiogram method may be applied to mine heart rates from previously collected accelerometery and expand our understanding of comparative cardiovascular physiology.
View details for DOI 10.1242/jeb.243872
View details for PubMedID 35502794
Scaling of maneuvering performance in baleen whales: larger whales outperform expectations.
The Journal of experimental biology
2022; 225 (5)
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.
View details for DOI 10.1242/jeb.243224
View details for PubMedID 35234874
Elephant seals time their long-distance migrations using a map sense
2022; 32 (4): R156-R157
View details for Web of Science ID 000771022000007
Elephant seals time their long-distance migrations using a map sense.
Current biology : CB
2022; 32 (4): R156-R157
Many marine animals migrate between foraging areas and reproductive sites, often timing the return migration with extreme precision. In theory, the decision to return should reflect energy acquisition at foraging areas, energetic costs associated with transit, and timing arrival for successful reproduction. For long-distance migrations to be successful, animals must integrate 'map' information to assess where they are relative to their reproductive site as well as 'calendar' information to know when to initiate the return migration given their distance from home1. Elephant seals, Mirounga angustirostris, migrate thousands of kilometers from reproductive sites to open ocean foraging areas (Figure 1A), yet return within a narrow window of time to specific beaches2. Each year, pregnant female elephant seals undertake a 240-day, 10,000 km foraging migration across the Northeast Pacific Ocean before returning to their breeding beaches, where they give birth 5 days after arriving2. We found that the seals' abilities to adjust the timing of their return migration is based on the perception of space and time, which further elucidates the mechanisms behind their astonishing navigational feats3.
View details for DOI 10.1016/j.cub.2022.01.031
View details for PubMedID 35231406
How Reproducibility Will Accelerate Discovery Through Collaboration in Physio-Logging.
Frontiers in physiology
2022; 13: 917976
What new questions could ecophysiologists answer if physio-logging research was fully reproducible? We argue that technical debt (computational hurdles resulting from prioritizing short-term goals over long-term sustainability) stemming from insufficient cyberinfrastructure (field-wide tools, standards, and norms for analyzing and sharing data) trapped physio-logging in a scientific silo. This debt stifles comparative biological analyses and impedes interdisciplinary research. Although physio-loggers (e.g., heart rate monitors and accelerometers) opened new avenues of research, the explosion of complex datasets exceeded ecophysiology's informatics capacity. Like many other scientific fields facing a deluge of complex data, ecophysiologists now struggle to share their data and tools. Adapting to this new era requires a change in mindset, from "data as a noun" (e.g., traits, counts) to "data as a sentence", where measurements (nouns) are associate with transformations (verbs), parameters (adverbs), and metadata (adjectives). Computational reproducibility provides a framework for capturing the entire sentence. Though usually framed in terms of scientific integrity, reproducibility offers immediate benefits by promoting collaboration between individuals, groups, and entire fields. Rather than a tax on our productivity that benefits some nebulous greater good, reproducibility can accelerate the pace of discovery by removing obstacles and inviting a greater diversity of perspectives to advance science and society. In this article, we 1) describe the computational challenges facing physio-logging scientists and connect them to the concepts of technical debt and cyberinfrastructure, 2) demonstrate how other scientific fields overcame similar challenges by embracing computational reproducibility, and 3) present a framework to promote computational reproducibility in physio-logging, and bio-logging more generally.
View details for DOI 10.3389/fphys.2022.917976
View details for PubMedID 35874548
Baleen whale inhalation variability revealed using animal-borne video tags.
2022; 10: e13724
Empirical metabolic rate and oxygen consumption estimates for free-ranging whales have been limited to counting respiratory events at the surface. Because these observations were limited and generally viewed from afar, variability in respiratory properties was unknown and oxygen consumption estimates assumed constant breath-to-breath tidal volume and oxygen uptake. However, evidence suggests that cetaceans in human care vary tidal volume and breathing frequency to meet aerobic demand, which would significantly impact energetic estimates if the findings held in free-ranging species. In this study, we used suction cup-attached video tags positioned posterior to the nares of two humpback whales (Megaptera novaeangliae) and four Antarctic minke whales (Balaenoptera bonaerensis) to measure inhalation duration, relative nares expansion, and maximum nares expansion. Inhalation duration and nares expansion varied between and within initial, middle, and terminal breaths of surface sequences between dives. The initial and middle breaths exhibited the least variability and had the shortest durations and smallest nares expansions. In contrast, terminal breaths were highly variable, with the longest inhalation durations and the largest nares expansions. Our results demonstrate breath-to-breath variability in duration and nares expansion, suggesting differential oxygen exchange in each breath during the surface interval. With future validation, inhalation duration or nares area could be used alongside respiratory frequency to improve oxygen consumption estimates by accounting for breath-to-breath variation in wild whales.
View details for DOI 10.7717/peerj.13724
View details for PubMedID 35880219
Baleen whale prey consumption based on high-resolution foraging measurements.
2021; 599 (7883): 85-90
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 430million 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*104tonnesironyr-1 in the Southern Ocean before whaling compared to 1.2*103tonnesironyr-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.
View details for DOI 10.1038/s41586-021-03991-5
View details for PubMedID 34732868
- Tools for integrating inertial sensor data with video bio-loggers, including estimation of animal orientation, motion, and position ANIMAL BIOTELEMETRY 2021; 9 (1)
Scaling of oscillatory kinematics and Froude efficiency in baleen whales.
The Journal of experimental biology
High efficiency lunate-tail swimming with high-aspect-ratio lifting surfaces has evolved in many vertebrate lineages, from fish to cetaceans. Baleen whales (Mysticeti) are the largest swimming animals that exhibit this locomotor strategy and present an ideal study system to examine how morphology and the kinematics of swimming scale to the largest body sizes. We used data from whale-borne inertial sensors coupled with morphometric measurements from aerial drones to calculate the hydrodynamic performance of oscillatory swimming in six baleen whale species ranging in body length from 5-25m (fin whale, Balaenoptera physalus; Bryde's whale, Balaenoptera edeni; sei whale, Balaenoptera borealis; Antarctic minke whales, Balaenoptera bonaerensis; humpback whales, Megaptera novaeangliae; and blue whales, Balaenoptera musculus). We find that mass-specific thrust increases with both swimming speed and body size. Froude efficiency, defined as the ratio of useful power output to the rate of energy input (Sloop, 1978), generally increased with swimming speed but decreased on average with increasing body size. This finding is contrary to previous results in smaller animals where Froude efficiency increased with body size. Although our empirically-parameterized estimates for swimming baleen whale drag was higher than that of a simple gliding model, oscillatory locomotion at this scale exhibits generally high Froude efficiency as in other adept swimmers. Our results quantify the fine-scale kinematics and estimate the hydrodynamics of routine and energetically expensive swimming modes at the largest scale.
View details for DOI 10.1242/jeb.237586
View details for PubMedID 34109418
- Modelling short-term energetic costs of sonar disturbance to cetaceans using high-resolution foraging data JOURNAL OF APPLIED ECOLOGY 2021
Cervical air sac oxygen profiles in diving emperor penguins: parabronchial ventilation and the respiratory oxygen store.
The Journal of experimental biology
Some marine birds and mammals can perform dives of extraordinary duration and depth. Such dive performance is dependent on many factors, including total body oxygen (O2) stores. For diving penguins, the respiratory system (air sacs and lungs) constitutes 30-50% of the total body O2 store. To better understand the role and mechanism of parabronchial ventilation and O2 utilization in penguins both on the surface and during the dive, we examined air sac partial pressures of O2 (PO2) in emperor penguins (Aptenodytes forsteri) equipped with backpack PO2 recorders. Cervical air sac PO2s at rest were lower than in other birds, while the cervical air sac to posterior thoracic air sac PO2 difference was larger. Pre-dive cervical air sac PO2s were often greater than those at rest, but had a wide range and were not significantly different from those at rest. The maximum respiratory O2 store and total body O2 stores calculated with representative anterior and posterior air sac PO2 data did not differ from prior estimates. The mean calculated anterior air sac O2 depletion rate for dives up to 11 min was approximately one-tenth that of the posterior air sacs. Low cervical air sac PO2s at rest may be secondary to a low ratio of parabronchial ventilation to parabronchial blood O2 extraction. During dives, overlap of simultaneously recorded cervical and posterior thoracic air sac PO2 profiles supported the concept of maintenance of parabronchial ventilation during a dive by air movement through the lungs.
View details for DOI 10.1242/jeb.230219
View details for PubMedID 33257430