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.
A perfectly inelastic collision: Bulk prey engulfment by baleen whales and dynamical implications for the world’s largest cetaceans
The largest animals are the rorquals, a group of whales which rapidly engulf large aggregations of small-bodied animals along with the water in which they are embedded, with the latter subsequently expulsed via filtration through baleen. Represented by species like the blue, fin, and humpback whales, rorquals can exist in a wide range of body lengths (8–30 m) and masses (4000–190,000 kg). When feeding on krill, kinematic data collected by whale-borne biologging sensors suggest that they first oscillate their flukes several times to accelerate towards their prey, followed by a coasting period with mouth agape as the prey-water mixture is engulfed in a process approximating a perfectly inelastic collision. These kinematic data, used along with momentum conservation and time-averages of a whale’s equation of motion, show the largest rorquals as generating significant body forces (10–40 kN) in order to set into forward motion enough engulfed
water to at least double overall mass. Interestingly, a scaling analysis of these equations suggests significant reductions in the amount of body force generated per kilogram of body mass at the larger sizes. In other words, and in concert with the allometric growth of the buccal cavity, gigantism would involve smaller fractions of muscle mass to engulf greater volumes of water and prey, thereby imparting a greater efficiency to this unique feeding strategy.
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- Award ID(s):
- 1656656
- NSF-PAR ID:
- 10207548
- Date Published:
- Journal Name:
- American journal of physics
- Volume:
- 88
- Issue:
- 10
- ISSN:
- 1943-2909
- Page Range / eLocation ID:
- 851 - 863
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis -
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.more » « less
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Abstract Microbial eukaryotes, critical links in aquatic food webs, are unicellular, but some, such as choanoflagellates, form multicellular colonies. Are there consequences to predator avoidance of being unicellular vs. forming larger colonies? Choanoflagellates share a common ancestor with animals and are used as model organisms to study the evolution of multicellularity. Escape in size from protozoan predators is suggested as a selective factor favoring evolution of multicellularity. Heterotrophic protozoans are categorized as suspension feeders, motile raptors, or passive predators that eat swimming prey which bump into them. We focused on passive predation and measured the mechanisms responsible for the susceptibility of unicellular vs. multicellular choanoflagellates,
Salpingoeca helianthica , to capture by passive heliozoan predators,Actinosphaerium nucleofilum , which trap prey on axopodia radiating from the cell body. Microvideography showed that unicellular and colonial choanoflagellates entered the predator's capture zone at similar frequencies, but a greater proportion of colonies contacted axopodia. However, more colonies than single cells were lost during transport by axopodia to the cell body. Thus, feeding efficiency (proportion of prey entering the capture zone that were engulfed in phagosomes) was the same for unicellular and multicellular prey, suggesting that colony formation is not an effective defense against such passive predators. -
The scale-dependence of locomotor performance has long been studied in comparative biomechanics, but how animals move in their natural environment remains poorly understood. At the upper extreme of body mass, baleen whales (Mysteci) are predictably among the most efficient swimmers in terms of cost of transport through a combination of low mass-specific metabolic rate and high hydrodynamic efficiency. Such efficiency enables these oceanic giants to migrate vast distances and thus underlies a major component of their life history and functional ecology. However, we lack even basic kinematic data for most species. Here we combine morphometric data from flyover drone photography, whale-borne inertial sensing tag data, and computational fluid dynamics (CFD) to study the locomotion of four rorqual species. Focusing on fundamental kinematic parameters such as tailbeat frequency and forward speed, we quantified spatial and temporal changes in swimming performance for individual whales and compared these metrics across a wide body mass range. We also calculated thrust and drag using lunate tail hydrodynamic modeling (Fish 1993), and compared these values against those from CFD simulations carried out with realistic rigid-body models. Differences in excess of 100% between the two approaches point to the significant contributions of tail and head heaving to overall drag, and thus the need to account for them in rigid-body CFD simulations. Together these kinematic data and CFD modeling inform a new parametric factor designed at multiplying the rigid-body drag equation to predict the contribution of body heaving unsteady hydrodynamics in cetaceans.more » « less
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Abstract Background Advances in biologging technology allow researchers access to previously unobservable behavioral states and movement patterns of marine animals. To relate behaviors with environmental variables, features must be evaluated at scales relevant to the animal or behavior. Remotely sensed environmental data, collected via satellites, often suffers from the effects of cloud cover and lacks the spatial or temporal resolution to adequately link with individual animal behaviors or behavioral bouts. This study establishes a new method for remotely and continuously quantifying surface ice concentration (SIC) at a scale relevant to individual whales using on-animal tag video data. Results Motion-sensing and video-recording suction cup tags were deployed on 7 Antarctic minke whales ( Balaenoptera bonaerensis ) around the Antarctic Peninsula in February and March of 2018. To compare the scale of camera-tag observations with satellite imagery, the area of view was simulated using camera-tag parameters. For expected conditions, we found the visible area maximum to be ~ 100m 2 which indicates that observations occur at an equivalent or finer scale than a single pixel of high-resolution visible spectrum satellite imagery. SIC was classified into one of six bins (0%, 1–20%, 21–40%, 41–60%, 61–80%, 81–100%) by two independent observers for the initial and final surfacing between dives. In the event of a disagreement, a third independent observer was introduced, and the median of the three observer’s values was used. Initial results ( n = 6) show that Antarctic minke whales in the coastal bays of the Antarctic Peninsula spend 52% of their time in open water, and only 15% of their time in water with SIC greater than 20%. Over time, we find significant variation in observed SIC, indicating that Antarctic minke occupy an extremely dynamic environment. Sentinel-2 satellite-based approaches of sea ice assessment were not possible because of persistent cloud cover during the study period. Conclusion Tag-video offers a means to evaluate ice concentration at spatial and temporal scales relevant to the individual. Combined with information on underwater behavior, our ability to quantify SIC continuously at the scale of the animal will improve upon current remote sensing methods to understand the link between animal behavior and these dynamic environmental variables.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1119/10.0001771
