Doctor of Philosophy, University of California Davis (2017)
Bachelor of Science, Cornell University (2010)
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
Towards a North Pacific Ocean long-term monitoring program for plastic pollution: A review and recommendations for plastic ingestion bioindicators.
Environmental pollution (Barking, Essex : 1987)
Marine debris is now a ubiquitous component of the Anthropocene global ocean. Plastic ingestion by marine wildlife was first reported in the 1960s and since that time, roughly one thousand marine species have been reported to consume this debris. This study focuses on plastic ingestion by marine invertebrates and vertebrates in the North Pacific Ocean. Specifically, we reviewed the scientific literature to assess the scope of the problem, identified key bioindicator species, and proposed guidelines for future monitoring of plastic debris in North Pacific marine ecosystems. Our meta-analysis confirmed that the North Pacific is among the most polluted ocean regions globally; roughly half of all fish and seabird specimens and more than three-quarters of sea turtles and bivalve specimens examined in this region had consumed plastic. While there are not enough standardized data to assess if these ingestion rates are worsening, sampling standardization and reporting of methods are improving over time. Using a rubric-evaluation approach, we evaluated 354 species for their potential to serve as bioindicators of the prevalence of plastic pollution in the North Pacific. This analysis revealed a suite of 12 bioindicator species candidates which sample a variety of ecosystem components and cover a wide range of plastic size classes. Thus, we contend that these bioindicator candidates provide a key foundation for developing a comprehensive plastic monitoring program in the region. To enhance the utility of these bioindicators, we developed a framework for standardized data collection to minimize methodological variabiloity across different studies and to facilitate the assessment of temporal trends over space and time. Tracking plastic ingestion by these bioindicators will help to assess the effectiveness of mitigation actions in the region, a critical step to evaluate progress towards sustainability and improved ocean health in the 21st century.
View details for DOI 10.1016/j.envpol.2022.119861
View details for PubMedID 35940480
Enhancing the ecological realism of evolutionary mismatch theory.
Trends in ecology & evolution
Following rapid environmental change, why do some animals thrive, while others struggle? We present an expanded, cue-response framework for predicting variation in behavioral responses to novel situations. We show how signal detection theory can be used when individuals have three behavioral options (approach, avoid, or ignore). Based on this theory, we outline predictions about which animals are more likely to make mistakes around novel conditions (i.e., fall for a trap or fail to use an undervalued resource) and the intensity of that mismatch (i.e., severe versus moderate). Explicitly considering three options provides a more holistic perspective and allows us to distinguish between severe and moderate traps, which could guide management strategies in a changing world.
View details for DOI 10.1016/j.tree.2021.10.011
View details for PubMedID 34802715
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
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
Plastic ingestion by marine fish is widespread and increasing.
Global change biology
Plastic pollution has pervaded almost every facet of the biosphere, yet we lack an understanding of consumption risk by marine species at the global scale. To address this, we compile data from research documenting plastic debris ingestion by marine fish, totaling 171,774 individuals of 555 species. Overall, 386 marine fish species have ingested plastic debris including 210 species of commercial importance. However, 148 species studied had no records of plastic consumption, suggesting that while this evolutionary trap is widespread, it is not yet universal. Across all studies that accounted for microplastics, the incidence rate of plastic ingested by fish was 26%. Over the last decade this incidence has doubled, increasing by 2.4±0.4%per year. This is driven both by increasing detection of smaller sized particles as a result of improved methodologies, as well as an increase in fish consuming plastic. Further, we investigated the role of geographic, ecological, and behavioral factors in the ingestion of plastic across species. These analyses revealed that the abundance of plastic in surface waters was positively correlated to plastic ingestion. Demersal species are more likely to ingest plastic in shallow waters; in contrast, pelagic species were most likely to consume plastic below the mixed layer. Mobile predatory species had the highest likelihood to ingest plastic; similarly, we found a positive relationship between trophic level and plastic ingestion. We also find evidence that surface ingestion-deep sea egestion of microplastics by mesopelagic myctophids is likely a key mechanism for the export of microplastics from the surface ocean to the seafloor, a sink for marine debris. These results elucidate the role of ecology and biogeography underlying plastic ingestion by marine fish and point toward species and regions in urgent need of study.
View details for DOI 10.1111/gcb.15533
View details for PubMedID 33561314
Microplastics and microfibers in surface waters of Monterey Bay National Marine Sanctuary, California.
Marine pollution bulletin
2021; 165: 112148
Despite a recent report of high concentrations of microplastics and microfibers in the mesopelagic waters of Monterey Bay National Marine Sanctuary (MBNMS), little is known about these particles in surface waters. From 2017 to 2019, we sampled two nearshore and two offshore locations within MBNMS using a manta trawl and analyzed these samples for microplastics and microfibers. We found an average concentration of 1.32 ± 0.70 (SE) particles per m3. We found the highest concentration of particles closest to shore, and the lowest concentration above the remote Davidson Seamount. Fiber-like debris was more common in offshore, as compared to nearshore, sites. Overall, particles in our samples were primarily buoyant synthetic polymers, including polypropylene and polyethylene. Our results provide baseline data on the degree of microplastic and microfiber pollution in MBNMS surface waters and confirm that this pollution can be found in waters from the surface to at least 1000 m depth.
View details for DOI 10.1016/j.marpolbul.2021.112148
View details for PubMedID 33610108
Lunge filter feeding biomechanics constrain rorqual foraging ecology across scale.
The Journal of experimental biology
Fundamental scaling relationships influence the physiology of vital rates, which in turn shape the ecology and evolution of organisms. For diving mammals, benefits conferred by large body size include reduced transport costs and enhanced breath-holding capacity, thereby increasing overall foraging efficiency. Rorqual whales feed by engulfing a large mass of prey-laden water at high speed and filtering it through baleen plates. However, as engulfment capacity increases with body length (Engulfment Volume Body Length 3.57), the surface area of the baleen filter does not increase proportionally (Baleen Area Body Length1.82), and thus the filtration time of larger rorquals predictably increases as the baleen surface area must filter a disproportionally large amount of water. We predicted that filtration time should scale with body length to the power of 1.75 (Filter Time Body Length1.75 ) We tested this hypothesis on four rorqual species using multi-sensor tags with corresponding unoccupied aircraft systems (UAS) -based body length estimates. We found that filter time scales with body length to the power of 1.79 (95% CI: 1.61 - 1.97). This result highlights a scale-dependent trade-off between engulfment capacity and baleen area that creates a biomechanical constraint to foraging through increased filtration time. Consequently, larger whales must target high density prey patches commensurate to the gulp size to meet their increased energetic demands. If these optimal patches are absent, larger rorquals may experience reduced foraging efficiency compared to smaller whales if they do not match their engulfment capacity to the size of targeted prey aggregations.
View details for DOI 10.1242/jeb.224196
View details for PubMedID 32820028
- Comprehensive bycatch assessment in US fisheries for prioritizing management NATURE SUSTAINABILITY 2020
Odors from marine plastic debris elicit foraging behavior in sea turtles.
Current biology : CB
2020; 30 (5): R213–R214
Pfaller et al. report that sea turtles respond to odors from biofouled plastic debris with the same behavior that is elicited by food odors, providing a possible unifying explanation for why sea turtles interact with marine plastic.
View details for DOI 10.1016/j.cub.2020.01.071
View details for PubMedID 32155421
Why whales are big but not bigger: Physiological drivers and ecological limits in the age of ocean giants.
Science (New York, N.Y.)
2019; 366 (6471): 1367–72
The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.
View details for DOI 10.1126/science.aax9044
View details for PubMedID 31831666
Extreme bradycardia and tachycardia in the world's largest animal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2019; 116 (50): 25329–32
The biology of the blue whale has long fascinated physiologists because of the animal's extreme size. Despite high energetic demands from a large body, low mass-specific metabolic rates are likely powered by low heart rates. Diving bradycardia should slow blood oxygen depletion and enhance dive time available for foraging at depth. However, blue whales exhibit a high-cost feeding mechanism, lunge feeding, whereby large volumes of prey-laden water are intermittently engulfed and filtered during dives. This paradox of such a large, slowly beating heart and the high cost of lunge feeding represents a unique test of our understanding of cardiac function, hemodynamics, and physiological limits to body size. Here, we used an electrocardiogram (ECG)-depth recorder tag to measure blue whale heart rates during foraging dives as deep as 184 m and as long as 16.5 min. Heart rates during dives were typically 4 to 8 beats min-1 (bpm) and as low as 2 bpm, while after-dive surface heart rates were 25 to 37 bpm, near the estimated maximum heart rate possible. Despite extreme bradycardia, we recorded a 2.5-fold increase above diving heart rate minima during the powered ascent phase of feeding lunges followed by a gradual decrease of heart rate during the prolonged glide as engulfed water is filtered. These heart rate dynamics explain the unique hemodynamic design in rorqual whales consisting of a large-diameter, highly compliant, elastic aortic arch that allows the aorta to accommodate blood ejected by the heart and maintain blood flow during the long and variable pauses between heartbeats.
View details for DOI 10.1073/pnas.1914273116
View details for Web of Science ID 000502577500056
View details for PubMedID 31767746
View details for PubMedCentralID PMC6911174
- Marine top predators as climate and ecosystem sentinels FRONTIERS IN ECOLOGY AND THE ENVIRONMENT 2019
- 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
Quantifying marine debris associated with coastal golf courses.
Marine pollution bulletin
2019; 140: 1–8
Identifying terrestrial sources of debris is essential to suppress the flow of plastic to the ocean. Here, we report a novel source of debris to the marine environment. From May 2016 to June 2018, we collected golf balls from coastal environments associated with five courses in Carmel, California. Our 75 collections recovered 39,602 balls from intertidal and nearshore environments adjacent to, or downriver from, the golf courses. Combining our collections with concurrent efforts of the Monterey Bay National Marine Sanctuary and the Pebble Beach Corporation, we report the retrieval of 50,681 balls, totaling approximately 2.5 tons of debris. We also examined decomposition patterns in the collected balls, which illustrate that degradation and loss of microplastic from golf balls to the marine environment may be of concern. Our findings will help to develop and direct mitigation procedures for this region and others with coastal golf courses.
View details for PubMedID 30803622
Scaling of swimming performance in baleen whales.
The Journal of experimental biology
The scale-dependence of locomotor factors have long been studied in comparative biomechanics, but remain poorly understood for animals at the upper extremes of body size. Rorqual baleen whales include the largest animals, but we lack basic kinematic data about their movements and behavior below the ocean surface. Here we combined morphometrics from aerial drone photogrammetry, whale-borne inertial sensing tag data, and hydrodynamic modeling to study the locomotion of five rorqual species. We quantified changes in tail oscillatory frequency and cruising speed for individual whales spanning a threefold variation in body length, corresponding to an order of magnitude variation in estimated body mass. Our results showed that oscillatory frequency decreases with body length (∝ length-0.53) while cruising speed remains roughly invariant (∝ length0.08) at 2 m s-1 We compared these measured results for oscillatory frequency against simplified models of an oscillating cantilever beam (∝ length-1) and an optimized oscillating Strouhal vortex generator (∝ length-1). The difference between our length-scaling exponent and the simplified models suggests that animals are often swimming non-optimally in order to feed or perform other routine behaviors. Cruising speed aligned more closely with an estimate of the optimal speed required to minimize the energetic cost of swimming (∝ length0.07). Our results are among the first to elucidate the relationships between both oscillatory frequency and cruising speed and body size for free-swimming animals at the largest scale.
View details for DOI 10.1242/jeb.204172
View details for PubMedID 31558588
The ecology of an olfactory trap.
Science (New York, N.Y.)
2018; 362 (6417): 904
View details for PubMedID 30467162
- Chemoattraction to dimethyl sulfide links the sulfur, iron, and carbon cycles in high-latitude oceans BIOGEOCHEMISTRY 2018; 138 (1): 1–21
Vertebrate prey in the diets of free-ranging kiwi (Apteryx spp.)
2018; 65 (4): 242–44
View details for Web of Science ID 000452190500008
- Odours from marine plastic debris induce food search behaviours in a forage fish PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 2017; 284 (1860)
Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds
2016; 2 (11): e1600395
Plastic debris is ingested by hundreds of species of organisms, from zooplankton to baleen whales, but how such a diversity of consumers can mistake plastic for their natural prey is largely unknown. The sensory mechanisms underlying plastic detection and consumption have rarely been examined within the context of sensory signals driving marine food web dynamics. We demonstrate experimentally that marine-seasoned microplastics produce a dimethyl sulfide (DMS) signature that is also a keystone odorant for natural trophic interactions. We further demonstrate a positive relationship between DMS responsiveness and plastic ingestion frequency using procellariiform seabirds as a model taxonomic group. Together, these results suggest that plastic debris emits the scent of a marine infochemical, creating an olfactory trap for susceptible marine wildlife.
View details for DOI 10.1126/sciadv.1600395
View details for Web of Science ID 000391267800007
View details for PubMedID 28861463
View details for PubMedCentralID PMC5569953
- We should not be afraid to talk about fear of failure in conservation BIOLOGICAL CONSERVATION 2016; 194: 218–19
- Fear of failure in conservation: The problem and potential solutions to aid conservation of extremely small populations BIOLOGICAL CONSERVATION 2015; 184: 209–17
Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2014; 111 (11): 4157–61
Tritrophic mutualistic interactions have been best studied in plant-insect systems. During these interactions, plants release volatiles in response to herbivore damage, which, in turn, facilitates predation on primary consumers or benefits the primary producer by providing nutrients. Here we explore a similar interaction in the Southern Ocean food web, where soluble iron limits primary productivity. Dimethyl sulfide has been studied in the context of global climate regulation and is an established foraging cue for marine top predators. We present evidence that procellariiform seabird species that use dimethyl sulfide as a foraging cue selectively forage on phytoplankton grazers. Their contribution of beneficial iron recycled to marine phytoplankton via excretion suggests a chemically mediated link between marine top predators and oceanic primary production.
View details for DOI 10.1073/pnas.1317120111
View details for Web of Science ID 000333027900063
View details for PubMedID 24591607
View details for PubMedCentralID PMC3964091
- NESTING DENSITY IS AN IMPORTANT FACTOR AFFECTING CHICK GROWTH AND SURVIVAL IN THE HERRING GULL CONDOR 2011; 113 (3): 565–71