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.
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Fast and Furious: Energetic Tradeoffs and Scaling of High-Speed Foraging in Rorqual Whales
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.
more » « less- NSF-PAR ID:
- 10371221
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative Organismal Biology
- Volume:
- 4
- Issue:
- 1
- ISSN:
- 2517-4843
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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The unique engulfment filtration strategy of microphagous rorqual whales has evolved relatively recently (<5 Ma) and exploits extreme predator/prey size ratios to overcome the maneuverability advantages of swarms of small prey, such as krill. Forage fish, in contrast, have been engaged in evolutionary arms races with their predators for more than 100 million years and have performance capabilities that suggest they should easily evade whale-sized predators, yet they are regularly hunted by some species of rorqual whales. To explore this phenomenon, we determined, in a laboratory setting, when individual anchovies initiated escape from virtually approaching whales, then used these results along with in situ humpback whale attack data to model how predator speed and engulfment timing affected capture rates. Anchovies were found to respond to approaching visual looming stimuli at expansion rates that give ample chance to escape from a sea lion-sized predator, but humpback whales could capture as much as 30–60% of a school at once because the increase in their apparent (visual) size does not cross their prey’s response threshold until after rapid jaw expansion. Humpback whales are, thus, incentivized to delay engulfment until they are very close to a prey school, even if this results in higher hydrodynamic drag. This potential exaptation of a microphagous filter feeding strategy for fish foraging enables humpback whales to achieve 7× the energetic efficiency (per lunge) of krill foraging, allowing for flexible foraging strategies that may underlie their ecological success in fluctuating oceanic conditions.
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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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Despite their enormous size, whales make their living as voracious predators. To catch their much smaller, more maneuverable prey, they have developed several unique locomotor strategies that require high energetic input, high mechanical power output and a surprising degree of agility. To better understand how body size affects maneuverability at the largest scale, we used bio-logging data, aerial photogrammetry and a high-throughput approach to quantify the maneuvering performance of seven species of free-swimming baleen whale. We found that as body size increases, absolute maneuvering performance decreases: larger whales use lower accelerations and perform slower pitch-changes, rolls and turns than smaller species. We also found that baleen whales exhibit positive allometry of maneuvering performance: relative to their body size, larger whales use higher accelerations, and perform faster pitch- changes, rolls and certain types of turns than smaller species. However, not all maneuvers were impacted by body size in the same way, and we found that larger whales behaviorally adjust for their decreased agility by using turns that they can perform more effectively. The positive allometry of maneuvering performance suggests that large whales have compensated for their increased body size by evolving more effective control surfaces and by preferentially selecting maneuvers that play to their strengths.more » « less
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Abstract Landscapes of fear describe a spatial representation of an animal's perceived risk of predation and the associated foraging costs, while energy landscapes describe the spatial representation of their energetic cost of moving and foraging. Fear landscapes are often dynamic and change based on predator presence and behaviour, and variation in abiotic conditions that modify risk. Energy landscapes are also dynamic and can change across diel, seasonal, and climatic timescales based on variability in temperature, snowfall, wind/current speeds, etc.
Recently, it was suggested that fear and energy landscapes should be integrated. In this paradigm, the interaction between landscapes relates to prey being forced to use areas of the energy landscape they would avoid if risk were not a factor. However, dynamic energy landscapes experienced by predators must also be considered since they can affect their ability to forage, irrespective of variation in prey behaviour. We propose an additional component to the fear and dynamic energy landscape paradigm that integrates landscapes of both prey and predators, where predator foraging behaviour is modulated by changes in their energyscape.
Specifically, we integrate the predator's energy landscape into foraging theory that predicts prey patch‐leaving decisions under the threat of predation. We predict that as a predator's energetic cost of foraging increases in a habitat, then the prey's foraging cost of predation and patch quitting harvest rate, will decrease. Prey may also decrease their vigilance in response to increased energetic foraging costs for predators, which will lower giving‐up densities of prey.
We then provide examples in terrestrial, aerial, and marine ecosystems where we might expect to see these effects. These include birds and sharks which use updrafts that vary based on wind and current speeds, tidal state, or temperature, and terrestrial predators (e.g. wolves) whose landscapes vary seasonally with snow depth or ice cover which may influence their foraging success and even diet selection.
A predator perspective is critical to considering the combination of these landscapes and their ecological consequences. Dynamic predator energy landscapes could add an additional spatiotemporal component to risk effects, which may cascade through food webs.
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