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.
Animals are distributed relative to the resources they rely upon, often scaling in abundance relative to available resources. Yet, in heterogeneously distributed environments, describing resource availability at relevant spatial scales remains a challenge in ecology, inhibiting understanding of predator distribution and foraging decisions. We investigated the foraging behaviour of two species of rorqual whales within spatially limited and numerically extraordinary super‐aggregations in two oceans. We additionally described the lognormal distribution of prey data at species‐specific spatial scales that matched the predator's unique lunge‐feeding strategy. Here we show that both humpback whales off South Africa's west coast and blue whales off the US west coast perform more lunges per unit time within these aggregations than when foraging individually, and that the biomass within gulp‐sized parcels was on average higher and more tightly distributed within super‐group‐associated prey patches, facilitating greater energy intake per feeding event as well as increased feeding rates. Prey analysis at predator‐specific spatial scales revealed a stronger association of super‐groups with patches containing relatively high geometric mean biomass and low geometric standard deviations than with arithmetic mean biomass, suggesting that the foraging decisions of rorqual whales may be more influenced by the distribution of high‐biomass portions of a patch than total biomass. The hierarchical distribution of prey in spatially restricted, temporally transient, super‐group‐associated patches demonstrated high biomass and less variable distributions that facilitated what are likely near‐minimum intervals between feeding events. Combining increased biomass with increased foraging rates implied that overall intake rates of whales foraging within super‐groups were approximately double those of whales foraging in other environments. Locating large, high‐quality prey patches via the detection of aggregation hotspots may be an important aspect of rorqual whale foraging, one that may have been suppressed when population sizes were anthropogenically reduced in the 20th century to critical lows. A free Plain Language Summary can be found within the Supporting Information of this article.
SignificanceWe present a major advancement in our ability to bring the physiological laboratory to the open ocean through the noninvasive use of a suction cup-attached tag equipped with surface electrodes. Our study provides heart rate data of a large, free-diving whale (blue whale) without prior capture or restraint. We recorded a wide range of heart rates from the tag, reaching only several beats per minute during deep foraging dives (bradycardia) and nearly 40 beats per minute at the sea surface (tachycardia) as the whale recovered from its oxygen debt. The latter likely represents maximal heart rate given the measured duration of the heart beat itself, thereby demonstrating the greatest dynamic range in cardiac activity at this scale.
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.
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.
The anatomy of large cetaceans has been well documented, mostly through dissection of dead specimens. However, the difficulty of studying the world's largest animals in their natural environment means the functions of anatomical structures must be inferred. Recently, non-invasive tracking devices have been developed that measure body position and orientation, thereby enabling the detailed reconstruction of underwater trajectories. The addition of cameras to the whale-borne tags allows the sensor data to be matched with real-time observations of how whales use their morphological structures, such as flukes, flippers, feeding apparatuses, and blowholes for the physiological functions of locomotion, feeding, and breathing. Here, we describe a new tag design with integrated video and inertial sensors and how it can be used to provide insights to the function of whale anatomy. This technology has the potential to facilitate a wide range of discoveries and comparative studies, but many challenges remain to increase the resolution and applicability of the data.
Bio-logging devices equipped with inertial measurement units—particularly accelerometers, magnetometers, and pressure sensors—have revolutionized our ability to study animals as necessary electronics have gotten smaller and more affordable over the last two decades. These animal-attached tags allow for fine scale determination of behavior in the absence of direct observation, particularly useful in the marine realm, where direct observation is often impossible, and recent devices can integrate more power hungry and sensitive instruments, such as hydrophones, cameras, and physiological sensors. To convert the raw voltages recorded by bio-logging sensors into biologically meaningful metrics of orientation (e.g., pitch, roll and heading), motion (e.g., speed, specific acceleration) and position (e.g., depth and spatial coordinates), we developed a series of MATLAB tools and online instructional tutorials. Our tools are adaptable for a variety of devices, though we focus specifically on the integration of video, audio, 3-axis accelerometers, 3-axis magnetometers, 3-axis gyroscopes, pressure, temperature, light and GPS data that are the standard outputs from Customized Animal Tracking Solutions (CATS) video tags. Our tools were developed and tested on cetacean data but are designed to be modular and adaptable for a variety of marine and terrestrial species. In this text, we describe how to use these tools, the theories and ideas behind their development, and ideas and additional tools for applying the outputs of the process to biological research. We additionally explore and address common errors that can occur during processing and discuss future applications. All code is provided open source and is designed to be useful to both novice and experienced programmers.
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