Honors & Awards
Terman Fellowship, Stanford University (2017-2020)
Young Investigator Award, Office of Naval Research (2016-2020)
Hoagland Award for Teaching Innovation, Vice Provost for Undergraduate Education, Humanities and Sciences Dean's Office, Stanford University (2015)
BSc, University of Texas at Austin, Zoology (2002)
MSc, Scripps Institution of Oceanography, University of California - San Diego, Marine Biology (2005)
PhD, University of British Columbia, Zoology (2010)
Independent Studies (7)
- Directed Instruction or Reading
BIOHOPK 198H (Aut, Win, Spr, Sum)
- Directed Reading in Biology
BIO 198 (Aut, Win, Spr)
- Graduate Research
BIO 300 (Aut, Win, Spr)
BIOHOPK 300H (Aut, Win, Spr, Sum)
- Teaching of Biological Science
BIOHOPK 290H (Win, Spr, Sum)
- Teaching of Biology
BIO 290 (Win)
- Undergraduate Research
BIOHOPK 199H (Aut, Win, Spr, Sum)
- Directed Instruction or Reading
Prior Year Courses
- Bio-logging and Bio-telemetry
BIOHOPK 14 (Spr)
BIOHOPK 84 (Spr)
- Topics in Comparative and Environmental Physiology
BIOHOPK 234H (Spr)
- Physiological Ecology of Marine Megafauna
BIOHOPK 179H, BIOHOPK 279H (Spr)
- Topics in Comparative and Environmental Physiology
BIOHOPK 234H (Spr)
- Bio-logging and Bio-telemetry
BIO 14 (Win)
- Bio-logging and Bio-telemetry
Doctoral Dissertation Reader (AC)
Ben Burford, William Oestreich
Postdoctoral Faculty Sponsor
Matthew Savoca, Paolo Segre
Doctoral Dissertation Advisor (AC)
David Cade, Max Czapanskiy, James Fahlbusch, Will Gough, Shirel Kahane-Rapport
David Cade, James Fahlbusch, Will Gough, Shirel Kahane-Rapport
- Memory and resource tracking drive blue whale migrations PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2019; 116 (12): 5582–87
Memory and resource tracking drive blue whale migrations.
Proceedings of the National Academy of Sciences of the United States of America
In terrestrial systems, the green wave hypothesis posits that migrating animals can enhance foraging opportunities by tracking phenological variation in high-quality forage across space (i.e., "resource waves"). To track resource waves, animals may rely on proximate cues and/or memory of long-term average phenologies. Although there is growing evidence of resource tracking in terrestrial migrants, such drivers remain unevaluated in migratory marine megafauna. Here we present a test of the green wave hypothesis in a marine system. We compare 10 years of blue whale movement data with the timing of the spring phytoplankton bloom resulting in increased prey availability in the California Current Ecosystem, allowing us to investigate resource tracking both contemporaneously (response to proximate cues) and based on climatological conditions (memory) during migrations. Blue whales closely tracked the long-term average phenology of the spring bloom, but did not track contemporaneous green-up. In addition, blue whale foraging locations were characterized by low long-term habitat variability and high long-term productivity compared with contemporaneous measurements. Results indicate that memory of long-term average conditions may have a previously underappreciated role in driving migratory movements of long-lived species in marine systems, and suggest that these animals may struggle to respond to rapid deviations from historical mean environmental conditions. Results further highlight that an ecological theory of migration is conserved across marine and terrestrial systems. Understanding the drivers of animal migration is critical for assessing how environmental changes will affect highly mobile fauna at a global scale.
View details for PubMedID 30804188
Physiological constraints on marine mammal body size
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2018; 115 (16): 3995–97
View details for PubMedID 29618615
Context-dependent lateralized feeding strategies in blue whales
2017; 27 (22): R1206–R1208
Lateralized behaviors benefit individuals by increasing task efficiency in foraging and anti-predator behaviors [1-4]. The conventional lateralization paradigm suggests individuals are left or right lateralized, although the direction of this laterality can vary for different tasks (e.g. foraging or predator inspection/avoidance). By fitting tri-axial movement sensors to blue whales (Balaenoptera musculus), and by recording the direction and size of their rolls during lunge feeding events, we show how these animals differ from such a paradigm. The strength and direction of individuals' lateralization were related to where and how the whales were feeding in the water column. Smaller rolls (≤180°) predominantly occurred at depth (>70 m), with whales being more likely to rotate clockwise around their longest axis (right lateralized). Larger rolls (>180°), conversely, occurred more often at shallower depths (<70 m) and were more likely to be performed anti-clockwise (left lateralized). More acrobatic rolls are typically used to target small, less dense krill patches near the water's surface [5,6], and we posit that the specialization of lateralized feeding strategies may enhance foraging efficiency in environments with heterogeneous prey distributions.
View details for PubMedID 29161554
A hydrodynamically active flipper-stroke in humpback whales
2017; 27 (13): R636–R637
A central paradigm of aquatic locomotion is that cetaceans use fluke strokes to power their swimming while relying on lift and torque generated by the flippers to perform maneuvers such as rolls, pitch changes and turns . Compared to other cetaceans, humpback whales (Megaptera novaeangliae) have disproportionately large flippers with added structural features to aid in hydrodynamic performance [2,3]. Humpbacks use acrobatic lunging maneuvers to attack dense aggregations of krill or small fish, and their large flippers are thought to increase their maneuverability and thus their ability to capture prey. Immediately before opening their mouths, humpbacks will often rapidly move their flippers, and it has been hypothesized that this movement is used to corral prey [4,5] or to generate an upward pitching moment to counteract the torque caused by rapid water engulfment . Here, we demonstrate an additional function for the rapid flipper movement during lunge feeding: the flippers are flapped using a complex, hydrodynamically active stroke to generate lift and increase propulsive thrust. We estimate that humpback flipper-strokes are capable of producing large forward oriented forces, which may be used to enhance lunge feeding performance. This behavior is the first observation of a lift-generating flipper-stroke for propulsion cetaceans and provides an additional function for the uniquely shaped humpback whale flipper.
View details for PubMedID 28697357
Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics.
Proceedings. Biological sciences
2017; 284 (1855)
Vertebrates have evolved to gigantic sizes repeatedly over the past 250 Myr, reaching their extreme in today's baleen whales (Mysticeti). Hypotheses for the evolution of exceptionally large size in mysticetes range from niche partitioning to predator avoidance, but there has been no quantitative examination of body size evolutionary dynamics in this clade and it remains unclear when, why or how gigantism evolved. By fitting phylogenetic macroevolutionary models to a dataset consisting of living and extinct species, we show that mysticetes underwent a clade-wide shift in their mode of body size evolution during the Plio-Pleistocene. This transition, from Brownian motion-like dynamics to a trended random walk towards larger size, is temporally linked to the onset of seasonally intensified upwelling along coastal ecosystems. High prey densities resulting from wind-driven upwelling, rather than abundant resources alone, are the primary determinant of efficient foraging in extant mysticetes and Late Pliocene changes in ocean dynamics may have provided an ecological pathway to gigantism in multiple independent lineages.
View details for DOI 10.1098/rspb.2017.0546
View details for PubMedID 28539520
How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration.
Annual review of marine science
2017; 9: 367-386
Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time.
View details for DOI 10.1146/annurev-marine-122414-033905
View details for PubMedID 27620830
Physical trade-offs shape the evolution of buoyancy control in sharks.
Proceedings. Biological sciences
2017; 284 (1866)
Buoyancy control is a fundamental aspect of aquatic life that has major implications for locomotor performance and ecological niche. Unlike terrestrial animals, the densities of aquatic animals are similar to the supporting fluid, thus even small changes in body density may have profound effects on locomotion. Here, we analysed the body composition (lipid versus lean tissue) of 32 shark species to study the evolution of buoyancy. Our comparative phylogenetic analyses indicate that although lean tissue displays minor positive allometry, liver volume exhibits pronounced positive allometry, suggesting that larger sharks evolved bulkier body compositions by adding lipid tissue to lean tissue rather than substituting lean for lipid tissue, particularly in the liver. We revealed a continuum of buoyancy control strategies that ranged from more buoyant sharks with larger livers in deeper ecosystems to relatively denser sharks with small livers in epipelagic habitats. Across this eco-morphological spectrum, our hydrodynamic modelling suggests that neutral buoyancy yields lower drag and more efficient steady swimming, whereas negative buoyancy may be more efficient during accelerated movements. The evolution of buoyancy control in sharks suggests that ecological and physiological factors mediate the selective pressures acting on these traits along two major gradients, body size and habitat depth.
View details for PubMedID 29118132
View details for PubMedCentralID PMC5698638
Kinematic Diversity in Rorqual Whale Feeding Mechanisms
2016; 26 (19): 2617-2624
Rorqual whales exhibit an extreme lunge filter-feeding strategy characterized by acceleration to high speed and engulfment of a large volume of prey-laden water [1-4]. Although tagging studies have quantified the kinematics of lunge feeding, the timing of engulfment relative to body acceleration has been modeled conflictingly because it could never be directly measured [5-7]. The temporal coordination of these processes has a major impact on the hydrodynamics and energetics of this high-cost feeding strategy [5-9]. If engulfment and body acceleration are temporally distinct, the overall cost of this dynamic feeding event would be minimized. However, greater temporal overlap of these two phases would theoretically result in higher drag and greater energetic costs. To address this discrepancy, we used animal-borne synchronized video and 3D movement sensors to quantify the kinematics of both the skull and body during feeding events. Krill-feeding blue and humpback whales exhibited temporally distinct acceleration and engulfment phases, with humpback whales reaching maximum gape earlier than blue whales. In these whales, engulfment coincided largely with body deceleration; however, humpback whales pursuing more agile fish demonstrated highly variable coordination of skull and body kinematics in the context of complex prey-herding techniques. These data suggest that rorquals modulate the coordination of acceleration and engulfment to optimize foraging efficiency by minimizing locomotor costs and maximizing prey capture. Moreover, this newfound kinematic diversity observed among rorquals indicates that the energetic efficiency of foraging is driven both by the whale's engulfment capacity and the comparative locomotor capabilities of predator and prey. VIDEO ABSTRACT.
View details for DOI 10.1016/j.cub.2016.07.037
View details for Web of Science ID 000385690800022
View details for PubMedID 27666966
Blue whales (Balaenoptera musculus) optimize foraging efficiency by balancing oxygen use and energy gain as a function of prey density.
2015; 1 (9)
Terrestrial predators can modulate the energy used for prey capture to maximize efficiency, but diving animals face the conflicting metabolic demands of energy intake and the minimization of oxygen depletion during a breath hold. It is thought that diving predators optimize their foraging success when oxygen use and energy gain act as competing currencies, but this hypothesis has not been rigorously tested because it has been difficult to measure the quality of prey that is targeted by free-ranging animals. We used high-resolution multisensor digital tags attached to foraging blue whales (Balaenoptera musculus) with concurrent acoustic prey measurements to quantify foraging performance across depth and prey density gradients. We parameterized two competing physiological models to estimate energy gain and expenditure based on foraging decisions. Our analyses show that at low prey densities, blue whale feeding rates and energy intake were low to minimize oxygen use, but at higher prey densities feeding frequency increased to maximize energy intake. Contrary to previous paradigms, we demonstrate that blue whales are not indiscriminate grazers but instead switch foraging strategies in response to variation in prey density and depth to maximize energetic efficiency.
View details for DOI 10.1126/sciadv.1500469
View details for PubMedID 26601290
View details for PubMedCentralID PMC4646804
Stretchy nerves are an essential component of the extreme feeding mechanism of rorqual whales
2015; 25 (9): R360-R361
Rorqual whales (Balaenopteridae) are among the largest vertebrates that have ever lived and include blue (Balaenoptera musculus) and fin (Balaenoptera physalus) whales. Rorquals differ from other baleen whales (Mysticeti) in possessing longitudinal furrows or grooves in the ventral skin that extend from the mouth to the umbilicus. This ventral grooved blubber directly relates to their intermittent lunge feeding strategy, which is unique among vertebrates and was potentially an evolutionary innovation that led to gigantism in this lineage . This strategy involves the rorqual whale rapidly engulfing a huge volume of prey-laden water and then concentrating the prey by more slowly expelling the water through baleen plates (Figure 1A). The volume of water engulfed during a lunge can exceed the volume of the whale itself . During engulfment, the whale accelerates, opens its jaw until it is almost perpendicular to the rostrum, and then the highly compliant floor of the oral cavity is inflated by the incoming water . The floor of the oral cavity expands by inversion of the tongue and ballooning of the adjacent floor of the mouth into the cavum ventrale, an immense fascial pocket between the body wall and overlying blubber layer that reaches as far back as the umbilicus. The ventral grooved blubber in fin whales expands by an estimated 162% in the circumferential direction and 38% longitudinally . In fin whales, multiple lunges can occur during a single dive, and the average time between lunges is just over forty seconds . Here, we show that nerves in the floor of the oral cavity of fin whales are highly extensible.
View details for Web of Science ID 000353999000007
View details for PubMedID 25942546
- Diving Behavior and Fine-Scale Kinematics of Free-Ranging Risso's Dolphins Foraging in Shallow and Deep-Water Habitats FRONTIERS IN ECOLOGY AND EVOLUTION 2019; 7
Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar.
The Journal of experimental biology
2019; 222 (Pt 5)
This study measured the degree of behavioral responses in blue whales (Balaenoptera musculus) to controlled noise exposure off the southern California coast. High-resolution movement and passive acoustic data were obtained from non-invasive archival tags (n=42) whereas surface positions were obtained with visual focal follows. Controlled exposure experiments (CEEs) were used to obtain direct behavioral measurements before, during and after simulated and operational military mid-frequency active sonar (MFAS), pseudorandom noise (PRN) and controls (no noise exposure). For a subset of deep-feeding animals (n=21), active acoustic measurements of prey were obtained and used as contextual covariates in response analyses. To investigate potential behavioral changes within individuals as a function of controlled noise exposure conditions, two parallel analyses of time-series data for selected behavioral parameters (e.g. diving, horizontal movement and feeding) were conducted. This included expert scoring of responses according to a specified behavioral severity rating paradigm and quantitative change-point analyses using Mahalanobis distance statistics. Both methods identified clear changes in some conditions. More than 50% of blue whales in deep-feeding states responded during CEEs, whereas no changes in behavior were identified in shallow-feeding blue whales. Overall, responses were generally brief, of low to moderate severity, and highly dependent on exposure context such as behavioral state, source-to-whale horizontal range and prey availability. Response probability did not follow a simple exposure-response model based on received exposure level. These results, in combination with additional analytical methods to investigate different aspects of potential responses within and among individuals, provide a comprehensive evaluation of how free-ranging blue whales responded to mid-frequency military sonar.
View details for PubMedID 30833464
- Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar JOURNAL OF EXPERIMENTAL BIOLOGY 2019; 222 (5)
Grouping reduces the metabolic demand of a social squid
Marine Ecology Progress Series
2019; 612: 141-150
View details for DOI 10.3354/meps12880
- Filtration area scaling and evolution in mysticetes: trophic niche partitioning and the curious cases of sei and pygmy right whales BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY 2018; 125 (2): 264–79
Allometric scaling of morphology and engulfment capacity in rorqual whales.
Journal of morphology
Body length is one of the most important factors that influence organismal function and ecological niche. Although larger animals tend to have a suite of physiological advantages, such as lower mass-specific metabolic rates and lower costs of transport, they may also experience significant limitations to unsteady locomotor performance or maneuverability because of the relative scaling of control surface areas and body mass. Rorqual whales are the largest of all animals and thus represent a unique study system for understanding how animals function at the extreme of body mass. Rorquals are characterized by an engulfment-filtration foraging strategy facilitated by a complex set of morphological adaptations. We studied the scaling of key morphological structures related to locomotion and feeding in six rorqual species in a comparative framework. Our analyses show that most rorqual species exhibit positive allometry of both the control surfaces and body length, but the large scaling differences between these parameters suggest that larger rorquals will predictably suffer from decreased maneuverability and unsteady locomotor performance. However, we found that the dimensions of the engulfment apparatus also exhibit positive allometry, and thus engulfment capacity was relatively greater in larger rorquals. We posit that the allometric growth in the engulfment apparatus may be an adaptation that ameliorates the detrimental effects of large size on maneuverability. Our analyses also reveal significant differences in the scaling of mass-specific engulfment capacity among rorqual species that may reflect the evolution of unique foraging behaviors and the exploitation of divergent ecological niches.
View details for PubMedID 30194740
A Dynamic State Model of Migratory Behavior and Physiology to Assess the Consequences of Environmental Variation and Anthropogenic Disturbance on Marine Vertebrates
2018; 191 (2): E40–E56
Integrating behavior and physiology is critical to formulating new hypotheses on the evolution of animal life-history strategies. Migratory capital breeders acquire most of the energy they need to sustain migration, gestation, and lactation before parturition. Therefore, when predicting the impact of environmental variation on such species, a mechanistic understanding of the physiology of their migratory behavior is required. Using baleen whales as a model system, we developed a dynamic state variable model that captures the interplay among behavioral decisions, energy, reproductive needs, and the environment. We applied the framework to blue whales (Balaenoptera musculus) in the eastern North Pacific Ocean and explored the effects of environmental and anthropogenic perturbations on female reproductive success. We demonstrate the emergence of migration to track prey resources, enabling us to quantify the trade-offs among capital breeding, body condition, and metabolic expenses. We predict that periodic climatic oscillations affect reproductive success less than unprecedented environmental changes do. The effect of localized, acute anthropogenic impacts depended on whales' behavioral response to the disturbance; chronic, but weaker, disturbances had little effect on reproductive success. Because we link behavior and vital rates by modeling individuals' energetic budgets, we provide a general framework to investigate the ecology of migration and assess the population consequences of disturbance, while identifying critical knowledge gaps.
View details for DOI 10.1086/695135
View details for Web of Science ID 000422944300002
View details for PubMedID 29351020
Determining forward speed from accelerometer jiggle in aquatic environments.
The Journal of experimental biology
2018; 221 (Pt 2)
How fast animals move is critical to understanding their energetic requirements, locomotor capacity and foraging performance, yet current methods for measuring speed via animal-attached devices are not universally applicable. Here, we present and evaluate a new method that relates forward speed to the stochastic motion of biologging devices as tag jiggle, the amplitude of the tag vibrations as measured by high sample rate accelerometers, increases exponentially with increasing speed. We successfully tested this method in a flow tank using two types of biologging devices and in situ on wild cetaceans spanning ∼3 to >20 m in length using two types of suction cup-attached tag and two types of dart-attached tag. This technique provides some advantages over other approaches for determining speed as it is device-orientation independent and relies only on a pressure sensor and a high sample rate accelerometer, sensors that are nearly universal across biologging device types.
View details for PubMedID 29191861
The evolution of foraging capacity and gigantism in cetaceans
Journal of Experimental Biology
View details for DOI 10.1242/jeb.166033
Resource partitioning facilitates coexistence in sympatric cetaceans in the California Current
ECOLOGY AND EVOLUTION
2017; 7 (21): 9085–97
Resource partitioning is an important process driving habitat use and foraging strategies in sympatric species that potentially compete. Differences in foraging behavior are hypothesized to contribute to species coexistence by facilitating resource partitioning, but little is known on the multiple mechanisms for partitioning that may occur simultaneously. Studies are further limited in the marine environment, where the spatial and temporal distribution of resources is highly dynamic and subsequently difficult to quantify. We investigated potential pathways by which foraging behavior may facilitate resource partitioning in two of the largest co-occurring and closely related species on Earth, blue (Balaenoptera musculus) and humpback (Megaptera novaeangliae) whales. We integrated multiple long-term datasets (line-transect surveys, whale-watching records, net sampling, stable isotope analysis, and remote-sensing of oceanographic parameters) to compare the diet, phenology, and distribution of the two species during their foraging periods in the highly productive waters of Monterey Bay, California, USA within the California Current Ecosystem. Our long-term study reveals that blue and humpback whales likely facilitate sympatry by partitioning their foraging along three axes: trophic, temporal, and spatial. Blue whales were specialists foraging on krill, predictably targeting a seasonal peak in krill abundance, were present in the bay for an average of 4.7 months, and were spatially restricted at the continental shelf break. In contrast, humpback whales were generalists apparently feeding on a mixed diet of krill and fishes depending on relative abundances, were present in the bay for a more extended period (average of 6.6 months), and had a broader spatial distribution at the shelf break and inshore. Ultimately, competition for common resources can lead to behavioral, morphological, and physiological character displacement between sympatric species. Understanding the mechanisms for species coexistence is both fundamental to maintaining biodiverse ecosystems, and provides insight into the evolutionary drivers of morphological differences in closely related species.
View details for PubMedID 29152200
Comparative Three-Dimensional Morphology of Baleen: Cross-Sectional Profiles and Volume Measurements Using CT Images
ANATOMICAL RECORD-ADVANCES IN INTEGRATIVE ANATOMY AND EVOLUTIONARY BIOLOGY
2017; 300 (11): 1942–52
Baleen whales are obligate filter feeders, straining prey-laden seawater through racks of keratinized baleen plates. Despite the importance of baleen to the ecology and natural history of these animals, relatively little work has been done on baleen morphology, particularly with regard to the three-dimensional morphology and structure of baleen. We used computed tomography (CT) scanning to take 3D images of six baleen specimens representing five species, including three complete racks. With these images, we described the three-dimensional shape of the baleen plates using cross-sectional profiles from within the gum tissue to the tip of the plates. We also measured the percentage of each specimen that was composed of either keratinized plate material or was void space between baleen plates, and thus available for seawater flow. Baleen plates have a complex three-dimensional structure with curvature that varies across the anterior-posterior, proximal-distal, and medial-lateral (lingual-labial) axes. These curvatures also vary with location along the baleen rack, and between species. Cross-sectional profiles resemble backwards-facing airfoils, and some specimens display S-shaped, or reflexed, camber. Within a baleen specimen, the intra-baleen void volume correlates with the average bristle diameter for a species, suggesting that essentially, thinner plates (with more space between them for flow) have thinner bristles. Both plate curvature and the relative proportions of plate and void volumes are likely to have implications for the mechanics of mysticete filtration, and future studies are needed to determine the particular functions of these morphological characters. Anat Rec, 300:1942-1952, 2017. © 2017 The Authors The Anatomical Record published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.
View details for PubMedID 28971628
View details for PubMedCentralID PMC5656919
Structure and Function in the Lunge Feeding Apparatus: Mechanical Properties of the Fin Whale Mandible
ANATOMICAL RECORD-ADVANCES IN INTEGRATIVE ANATOMY AND EVOLUTIONARY BIOLOGY
2017; 300 (11): 1953–62
The mandibles of rorqual whales are highly modified to support loads associated with lunge-feeding, a dynamic filter feeding mechanism that is characterized by rapid changes in gape angle and acceleration. Although these structures are the largest ossified elements in animals and an important part of the rorqual engulfment apparatus, details of internal structure are limited and no direct measurements of mechanical properties exist. Likewise, the forces that are sustained by the mandibles are unknown. Here we report on the structure and mechanical behavior of the mandible of an adult fin whale. A series of transverse sections were cut at locations along the entire length of a 3.6-m left mandible recovered post-mortem from a 16-m fin whale, and CT scanned to make density maps. Cored samples 6-8 mm in diameter were tested in compression to determine the Young's modulus and strength. In addition, wet density, dry density and mineral density were measured. Dense cortical bone occupies only a relatively narrow peripheral layer while much less dense and oil-filled trabecular bone occupies the rest. Mineral density of both types is strongly correlated with dry density and CT Hounsfield units. Compressive strength is strongly correlated with Young's modulus, while strength and stiffness are both correlated with mineral density. It appears that the superficial compact layer is the main load bearing element, and that the mandible is reinforced against dorso-vental flexion that would occur during the peak loads while feeding. Anat Rec, 300:1953-1962, 2017. © 2017 Wiley Periodicals, Inc.
View details for PubMedID 28971624
Avoidance responses of minke whales to 1-4kHz naval sonar.
Marine pollution bulletin
Minke whales are difficult to study and little information exists regarding their responses to anthropogenic sound. This study pools data from behavioural response studies off California and Norway. Data are derived from four tagged animals, of which one from each location was exposed to naval sonar signals. Statistical analyses were conducted using Mahalanobis distance to compare overall changes in parameters summarising dive behaviour, avoidance behaviour, and potential energetic costs of disturbance. Our quantitative analysis showed that both animals initiated avoidance behaviour, but responses were not associated with unusual dive behaviour. In one exposed animal the avoidance of the sonar source included a 5-fold increase in horizontal speed away from the source, implying a significant increase in metabolic rate. Despite the different environmental settings and exposure contexts, clear changes in behaviour were observed providing the first insights into the nature of responses to human noise for this wide-ranging species.
View details for DOI 10.1016/j.marpolbul.2017.05.037
View details for PubMedID 28552251
- A MULTIVARIATE MIXED HIDDEN MARKOV MODEL FOR BLUE WHALE BEHAVIOUR AND RESPONSES TO SOUND EXPOSURE ANNALS OF APPLIED STATISTICS 2017; 11 (1): 362-392
Kinematics of ram filter feeding and beat–glide swimming in the northern anchovy Engraulis mordax
Journal of Experimental Biology
2017; 220: 2717-2725
View details for DOI 10.1242/jeb.158337
Hydrodynamic properties of fin whale flippers predict maximum rolling performance.
journal of experimental biology
2016; 219: 3315-3320
Maneuverability is one of the most important and least understood aspects of animal locomotion. The hydrofoil-like flippers of cetaceans are thought to function as control surfaces that effect maneuvers, but quantitative tests of this hypothesis have been lacking. Here, we constructed a simple hydrodynamic model to predict the longitudinal-axis roll performance of fin whales, and we tested its predictions against kinematic data recorded by on-board movement sensors from 27 free-swimming fin whales. We found that for a given swimming speed and roll excursion, the roll velocity of fin whales calculated from our field data agrees well with that predicted by our hydrodynamic model. Although fluke and body torsion may further influence performance, our results indicate that lift generated by the flippers is sufficient to drive most of the longitudinal-axis rolls used by fin whales for feeding and maneuvering.
View details for PubMedID 27591304
- How to tag a jellyfish? A methodological review and guidelines to successful jellyfish tagging JOURNAL OF PLANKTON RESEARCH 2016; 38 (6): 1347-1363
- Studying cetacean behaviour: new technological approaches and conservation applications ANIMAL BEHAVIOUR 2016; 120: 235-244
- Development of an automated method of detecting stereotyped feeding events in multisensor data from tagged rorqual whales ECOLOGY AND EVOLUTION 2016; 6 (20): 7522-7535
- Discrimination of fast click-series produced by tagged Risso's dolphins (Grampus griseus) for echolocation or communication JOURNAL OF EXPERIMENTAL BIOLOGY 2016; 219 (18): 2898-2907
Prey-mediated behavioral responses of feeding blue whales in controlled sound exposure experiments
2016; 26 (4): 1075-1085
Behavioral response studies provide significant insights into the nature, magnitude, and consequences of changes in animal behavior in response to some external stimulus. Controlled exposure experiments (CEEs) to study behavioral response have faced challenges in quantifying the importance of and interaction among individual variability, exposure conditions, and environmental covariates. To investigate these complex parameters relative to blue whale behavior and how it may change as a function of certain sounds, we deployed multi-sensor acoustic tags and conducted CEEs using simulated mid-frequency active sonar (MFAS) and pseudo-random noise (PRN) stimuli, while collecting synoptic, quantitative prey measures. In contrast to previous approaches that lacked such prey data, our integrated approach explained substantially more variance in blue whale dive behavioral responses to mid-frequency sounds (r2 = 0.725 vs. 0.14 previously). Results demonstrate that deep-feeding whales respond more clearly and strongly to CEEs than those in other behavioral states, but this was only evident with the increased explanatory power provided by incorporating prey density and distribution as contextual covariates. Including contextual variables increases the ability to characterize behavioral variability and empirically strengthens previous findings that deep-feeding blue whales respond significantly to mid-frequency sound exposure. However, our results are only based on a single behavioral state with a limited sample size, and this analytical framework should be applied broadly across behavioral states. The increased capability to describe and account for individual response variability by including environmental variables, such as prey, that drive foraging behavior underscores the importance of integrating these and other relevant contextual parameters in experimental designs. Our results suggest the need to measure and account for the ecological dynamics of predator-prey interactions when studying the effects of anthropogenic disturbance in feeding animals.
View details for DOI 10.1002/15-0783
View details for Web of Science ID 000378092900009
View details for PubMedID 27509749
Multiple-stage decisions in a marine central-place forager
ROYAL SOCIETY OPEN SCIENCE
2016; 3 (5)
Air-breathing marine animals face a complex set of physical challenges associated with diving that affect the decisions of how to optimize feeding. Baleen whales (Mysticeti) have evolved bulk-filter feeding mechanisms to efficiently feed on dense prey patches. Baleen whales are central place foragers where oxygen at the surface represents the central place and depth acts as the distance to prey. Although hypothesized that baleen whales will target the densest prey patches anywhere in the water column, how depth and density interact to influence foraging behaviour is poorly understood. We used multi-sensor archival tags and active acoustics to quantify Antarctic humpback whale foraging behaviour relative to prey. Our analyses reveal multi-stage foraging decisions driven by both krill depth and density. During daylight hours when whales did not feed, krill were found in deep high-density patches. As krill migrated vertically into larger and less dense patches near the surface, whales began to forage. During foraging bouts, we found that feeding rates (number of feeding lunges per hour) were greatest when prey was shallowest, and feeding rates decreased with increasing dive depth. This strategy is consistent with previous models of how air-breathing diving animals optimize foraging efficiency. Thus, humpback whales forage mainly when prey is more broadly distributed and shallower, presumably to minimize diving and searching costs and to increase feeding rates overall and thus foraging efficiency. Using direct measurements of feeding behaviour from animal-borne tags and prey availability from echosounders, our study demonstrates a multi-stage foraging process in a central place forager that we suggest acts to optimize overall efficiency by maximizing net energy gain over time. These data reveal a previously unrecognized level of complexity in predator-prey interactions and underscores the need to simultaneously measure prey distribution in marine central place forager studies.
View details for DOI 10.1098/rsos.160043
View details for Web of Science ID 000377969800009
View details for PubMedID 27293784
View details for PubMedCentralID PMC4892446
Development of an automated method of detecting stereotyped feeding events in multisensor data from tagged rorqual whales.
Ecology and evolution
2016; 6 (20): 7522–35
The introduction of animal-borne, multisensor tags has opened up many opportunities for ecological research, making previously inaccessible species and behaviors observable. The advancement of tag technology and the increasingly widespread use of bio-logging tags are leading to large volumes of sometimes extremely detailed data. With the increasing quantity and duration of tag deployments, a set of tools needs to be developed to aid in facilitating and standardizing the analysis of movement sensor data. Here, we developed an observation-based decision tree method to detect feeding events in data from multisensor movement tags attached to fin whales (Balaenoptera physalus). Fin whales exhibit an energetically costly and kinematically complex foraging behavior called lunge feeding, an intermittent ram filtration mechanism. Using this automated system, we identified feeding lunges in 19 fin whales tagged with multisensor tags, during a total of over 100 h of continuously sampled data. Using movement sensor and hydrophone data, the automated lunge detector correctly identified an average of 92.8% of all lunges, with a false-positive rate of 9.5%. The strong performance of our automated feeding detector demonstrates an effective, straightforward method of activity identification in animal-borne movement tag data. Our method employs a detection algorithm that utilizes a hierarchy of simple thresholds based on knowledge of observed features of feeding behavior, a technique that is readily modifiable to fit a variety of species and behaviors. Using automated methods to detect behavioral events in tag records will significantly decrease data analysis time and aid in standardizing analysis methods, crucial objectives with the rapidly increasing quantity and variety of on-animal tag data. Furthermore, our results have implications for next-generation tag design, especially long-term tags that can be outfitted with on-board processing algorithms that automatically detect kinematic events and transmit ethograms via acoustic or satellite telemetry.
View details for PubMedID 28725418
View details for PubMedCentralID PMC5513260
- Using morphology to infer physiology: case studies on rorqual whales (Balaenopteridae) CANADIAN JOURNAL OF ZOOLOGY 2015; 93 (9): 687-700
- Prey density and distribution drive the three-dimensional foraging strategies of the largest filter feeder FUNCTIONAL ECOLOGY 2015; 29 (7): 951-961
Mechanical challenges to freshwater residency in sharks and rays.
journal of experimental biology
2015; 218: 1099-1110
Major transitions between marine and freshwater habitats are relatively infrequent, primarily as a result of major physiological and ecological challenges. Few species of cartilaginous fish have evolved to occupy freshwater habitats. Current thought suggests that the metabolic physiology of sharks has remained a barrier to the diversification of this taxon in freshwater ecosystems. Here, we demonstrate that the physical properties of water provide an additional constraint for this species-rich group to occupy freshwater systems. Using hydromechanical modeling, we show that occurrence in fresh water results in a two- to three-fold increase in negative buoyancy for sharks and rays. This carries the energetic cost of lift production and results in increased buoyancy-dependent mechanical power requirements for swimming and increased optimal swim speeds. The primary source of buoyancy, the lipid-rich liver, offers only limited compensation for increased negative buoyancy as a result of decreasing water density; maintaining the same submerged weight would involve increasing the liver volume by very large amounts: 3- to 4-fold in scenarios where liver density is also reduced to currently observed minimal levels and 8-fold without any changes in liver density. The first data on body density from two species of elasmobranch occurring in freshwater (the bull shark Carcharhinus leucas, Müller and Henle 1839, and the largetooth sawfish Pristis pristis, Linnaeus 1758) support this hypothesis, showing similar liver sizes as marine forms but lower liver densities, but the greatest negative buoyancies of any elasmobranch studied to date. Our data suggest that the mechanical challenges associated with buoyancy control may have hampered the invasion of freshwater habitats in elasmobranchs, highlighting an additional key factor that may govern the predisposition of marine organisms to successfully establish in freshwater habitats.
View details for DOI 10.1242/jeb.114868
View details for PubMedID 25573824
- Feeding performance by sympatric blue and fin whales exploiting a common prey resource MARINE MAMMAL SCIENCE 2015; 31 (1): 345-354
- Formal Comment on Schorr GS, Falcone EA, Moretti DJ, Andrews RD (2014) First Long-Term Behavioral Records from Cuvier's Beaked Whales (Ziphius cavirostris) Reveal Record-Breaking Dives. PLoS ONE 9(3): e92633. doi:10.1371/journal.pone.0092633. PloS one 2015; 10 (12): e0142287
- Simultaneous tracking of blue whales and large ships demonstrates limited behavioral responses for avoiding collision ENDANGERED SPECIES RESEARCH 2015; 27 (3): 219-232
- Acoustic and foraging behavior of a Baird's beaked whale, Berardius bairdii, exposed to simulated sonar SCIENTIFIC REPORTS 2014; 4
Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis).
journal of experimental biology
2014; 217: 2851-2854
Body size and feeding mode are two fundamental characteristics that determine foraging performance and ecological niche. As the smallest obligate lunge filter feeders, minke whales represent an ideal system for studying the physical and energetic limits of filter feeding in endotherms. We used multi-sensor suction cup tags to quantify the feeding performance of Antarctic minke whales. Foraging dives around and beneath sea ice contained up to 24 lunges per dive, the highest feeding rates for any lunge-feeding whale. Their small size allows minke whales access to krill in sea-ice environments not easily accessible to larger baleen whales. Furthermore, their ability to filter feed provides an advantage over other smaller sympatric krill predators such as penguins and seals that feed on individual prey. The unique combination of body size, feeding mechanism and sea-ice habitat of Antarctic minke whales defines a previously undocumented energetic niche that is unique among aquatic vertebrates.
View details for DOI 10.1242/jeb.106682
View details for PubMedID 25122916
Using accelerometers to determine the calling behavior of tagged baleen whales.
journal of experimental biology
2014; 217: 2449-2455
Low-frequency acoustic signals generated by baleen whales can propagate over vast distances, making the assignment of calls to specific individuals problematic. Here, we report the novel use of acoustic recording tags equipped with high-resolution accelerometers to detect vibrations from the surface of two tagged fin whales that directly match the timing of recorded acoustic signals. A tag deployed on a buoy in the vicinity of calling fin whales and a recording from a tag that had just fallen off a whale were able to detect calls acoustically but did not record corresponding accelerometer signals that were measured on calling individuals. Across the hundreds of calls measured on two tagged fin whales, the accelerometer response was generally anisotropic across all three axes, appeared to depend on tag placement and increased with the level of received sound. These data demonstrate that high-sample rate accelerometry can provide important insights into the acoustic behavior of baleen whales that communicate at low frequencies. This method helps identify vocalizing whales, which in turn enables the quantification of call rates, a fundamental component of models used to estimate baleen whale abundance and distribution from passive acoustic monitoring.
View details for DOI 10.1242/jeb.103259
View details for PubMedID 24803468
- The device that revolutionized marine organismal biology. journal of experimental biology 2014; 217: 167-168
- Tracking fitness in marine vertebrates: current knowledge and opportunities for future research MARINE ECOLOGY PROGRESS SERIES 2014; 496: 1-17