Microparticles, such as microplastics and microfibers, are ubiquitous in marine food webs. Filter-feeding megafauna may be at extreme risk of exposure to microplastics, but neither the amount nor ...pathway of microplastic ingestion are well understood. Here, we combine depth-integrated microplastic data from the California Current Ecosystem with high-resolution foraging measurements from 191 tag deployments on blue, fin, and humpback whales to quantify plastic ingestion rates and routes of exposure. We find that baleen whales predominantly feed at depths of 50-250 m, coinciding with the highest measured microplastic concentrations in the pelagic ecosystem. Nearly all (99%) microplastic ingestion is predicted to occur via trophic transfer. We predict that fish-feeding whales are less exposed to microplastic ingestion than krill-feeding whales. Per day, a krill-obligate blue whale may ingest 10 million pieces of microplastic, while a fish-feeding humpback whale likely ingests 200,000 pieces of microplastic. For species struggling to recover from historical whaling alongside other anthropogenic pressures, our findings suggest that the cumulative impacts of multiple stressors require further attention.
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.
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 mand 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.
Lunge feeding by rorqual whales (Balaenopteridae) is associated with a high energetic cost that decreases diving capacity, thereby limiting access to dense prey patches at depth. Despite this cost, ...rorquals exhibit high rates of lipid deposition and extremely large maximum body size. To address this paradox, we integrated kinematic data from digital tags with unsteady hydrodynamic models to estimate the energy budget for lunges and foraging dives of blue whales (Balaenoptera musculus), the largest rorqual and living mammal. Our analysis suggests that, despite the large amount of mechanical work required to lunge feed, a large amount of prey and, therefore, energy is obtained during engulfment. Furthermore, we suggest that foraging efficiency for blue whales is significantly higher than for other marine mammals by nearly an order of magnitude, but only if lunges target extremely high densities of krill. The high predicted efficiency is attributed to the enhanced engulfment capacity, rapid filter rate and low mass-specific metabolic rate associated with large body size in blue whales. These results highlight the importance of high prey density, regardless of prey patch depth, for efficient bulk filter feeding in baleen whales and may explain some diel changes in foraging behavior in rorqual whales.
Abstract
Blue whales are often characterized as highly stable, open-ocean swimmers who sacrifice maneuverability for long-distance cruising performance. However, recent studies have revealed that ...blue whales actually exhibit surprisingly complex underwater behaviors, yet little is known about the performance and control of these maneuvers. Here, we use multi-sensor biologgers equipped with cameras to quantify the locomotor dynamics and the movement of the control surfaces used by foraging blue whales. Our results revealed that simple maneuvers (rolls, turns, and pitch changes) are performed using distinct combinations of control and power provided by the flippers, the flukes, and bending of the body, while complex trajectories are structured by combining sequences of simple maneuvers. Furthermore, blue whales improve their turning performance by using complex banked turns to take advantage of their substantial dorso-ventral flexibility. These results illustrate the important role body flexibility plays in enhancing control and performance of maneuvers, even in the largest of animals. The use of the body to supplement the performance of the hydrodynamically active surfaces may represent a new mechanism in the control of aquatic locomotion.
We quantified the relative influence of maternal fidelity to feeding grounds and natal fidelity to breeding grounds on the population structure of humpback whales Megaptera novaeangliae based on an ...ocean-wide survey of mitochondrial (mt) DNA diversity in the North Pacific. For 2193 biopsy samples collected from whales in 10 feeding regions and 8 breeding regions during the winter and summer of 2004 to 2006, we first used microsatellite genotyping (average, 9.5 loci) to identify replicate samples. From sequences of the mtDNA control region (500 bp) we identified 28 unique haplotypes from 30 variable sites. Haplotype frequencies differed markedly among feeding regions (overall F
ST = 0.121, ΦST = 0.178, p < 0.0001), supporting previous evidence of strong maternal fidelity. Haplotype frequencies also differed markedly among breeding regions (overall F
ST = 0.093, ΦST = 0.106, p < 0.0001), providing evidence of strong natal fidelity. Although sex-biased dispersal was not evident, differentiation of microsatellite allele frequencies was weak compared to differentiation of mtDNA haplotypes, suggesting male-biased gene flow. Feeding and breeding regions showed significant differences in haplotype frequencies, even for regions known to be strongly connected by patterns of individual migration. Thus, the influence of migratory fidelity seems to operate somewhat independently on feeding and breeding grounds over an evolutionary time scale. This results in a complex population structure and the potential to define multiple units to conserve in either seasonal habitat.
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.
Beaked whales are hypothesized to be particularly sensitive to anthropogenic noise, based on previous strandings and limited experimental and observational data. However, few species have been ...studied in detail. We describe the underwater behavior of a Baird's beaked whale (Berardius bairdii) from the first deployment of a multi-sensor acoustic tag on this species. The animal exhibited shallow (23 ± 15 m max depth), intermediate (324 ± 49 m), and deep (1138 ± 243 m) dives. Echolocation clicks were produced with a mean inter-click interval of approximately 300 ms and peak frequency of 25 kHz. Two deep dives included presumed foraging behavior, with echolocation pulsed sounds (presumed prey capture attempts) associated with increased maneuvering, and sustained inverted swimming during the bottom phase of the dive. A controlled exposure to simulated mid-frequency active sonar (3.5-4 kHz) was conducted 4 hours after tag deployment, and within 3 minutes of exposure onset, the tagged whale increased swim speed and body movement, and continued to show unusual dive behavior for each of its next three dives, one of each type. These are the first data on the acoustic foraging behavior in this largest beaked whale species, and the first experimental demonstration of a response to simulated sonar.
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
), the surface area of the baleen filter does not increase proportionally (baleen area∝body length
), 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 length
). We tested this hypothesis on four rorqual species using multi-sensor tags with corresponding unoccupied aircraft systems-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 with smaller whales if they do not match their engulfment capacity to the size of targeted prey aggregations.
Marine spatial planning provides a comprehensive framework for managing multiple uses of the marine environment and has the potential to minimize environmental impacts and reduce conflicts among ...users. Spatially explicit assessments of the risks to key marine species from human activities are a requirement of marine spatial planning. We assessed the risk of ships striking humpback (Megaptera novaeangliae), blue (Balaenoptera musculus), and fin (Balaenoptera physalus) whales in alternative shipping routes derived from patterns of shipping traffic off Southern California (U.S.A.). Specifically, we developed whale-habitat models and assumed ship-strike risk for the alternative shipping routes was proportional to the number of whales predicted by the models to occur within each route. This definition of risk assumes all ships travel within a single route. We also calculated risk assuming ships travel via multiple routes. We estimated the potential for conflict between shipping and other uses (military training and fishing) due to overlap with the routes. We also estimated the overlap between shipping routes and protected areas. The route with the lowest risk for humpback whales had the highest risk for fin whales and vice versa. Risk to both species may be ameliorated by creating a new route south of the northern Channel Islands and spreading traffic between this new route and the existing route in the Santa Barbara Channel. Creating a longer route may reduce the overlap between shipping and other uses by concentrating shipping traffic. Blue whales are distributed more evenly across our study area than humpback and fin whales; thus, risk could not be ameliorated by concentrating shipping traffic in any of the routes we considered. Reducing ship-strike risk for blue whales may be necessary because our estimate of the potential number of strikes suggests that they are likely to exceed allowable levels of anthropogenic impacts established under U.S. laws. La planificación marina espacial proporciona un marco de referencia integral para el manejo de usos múltiples del ambiente marino, y tiene el potencial para minimizar los efectos ambientales y reducir conflictos entre los usuarios. Las evaluaciones espacialmente explícitas de los riesgos para especies marinas clave derivados de las actividades humanas son un requerimiento de la planificación marina espacial. Evaluamos el riesgo de colisión de barcos con ballenas Megaptera novaeangliae, Balaenoptera musculus y B. physalus en rutas de navegación alternas derivadas de patrones del tráfico marino en el sur de California (U.S.A.). Específicamente, desarrollamos modelos del hábitat de ballenas y asumimos que el riesgo de colisión con barcos en las rutas alternativas fue proporcional al número de ballenas que los modelos pronosticaron que iban a ocurrir en cada ruta. Esta definición de riesgo asume que todos los barcos viajan en una sola ruta. También calculamos el riesgo asumiendo que los barcos viajan en rutas múltiples. Estimamos el potencial de conflictos entre la navegación y otros usos (entrenamiento militar y pesca) debido al traslape con las rutas. También estimamos el traslape entre rutas de navegación y áreas protegidas. La ruta con el menor riesgo para M. novaeangliae tenía el mayor riesgo para B. physalus y viceversa. El riesgo para ambas especies puede ser disminuido mediante la creación de una nueva ruta al sur de las Channel Islands y distribuyendo el tráfico entre esta ruta nueva y la existente en el Canal de Santa Bárbara. La creación de una ruta más larga puede reducir el traslape entre la navegación y otros usos al concentrar el tráfico de navegación. Las ballenas B. musculus se distribuyen más homogéneamente que M. novaeangliae y B. physalus en nuestra zona de estudio; por lo tanto, el riesgo no podría disminuir con la concentración del tráfico de navegación en ninguna de las rutas que consideramos. La reducción del riesgo de colisión de las ballenas puede ser necesario porque nuestra evaluación del número potencial de choques sugiere que es probable que excedan los niveles permisibles de impactos antropogénicos establecidos por las leyes de E.U.A.
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