William T Gough, David E Cade, Max F Czapanskiy, Jean Potvin, Frank E Fish, Shirel R Kahane-Rapport, Matthew S Savoca, K C Bierlich, David W Johnston, Ari S Friedlaender, Andy Szabo, Lars Bejder, Jeremy A Goldbogen
{"title":"Fast and Furious: Energetic Tradeoffs and Scaling of High-Speed Foraging in Rorqual Whales.","authors":"William T Gough, David E Cade, Max F Czapanskiy, Jean Potvin, Frank E Fish, Shirel R Kahane-Rapport, Matthew S Savoca, K C Bierlich, David W Johnston, Ari S Friedlaender, Andy Szabo, Lars Bejder, Jeremy A Goldbogen","doi":"10.1093/iob/obac038","DOIUrl":null,"url":null,"abstract":"<p><p>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<sup>-1</sup>) 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.</p>","PeriodicalId":13666,"journal":{"name":"Integrative Organismal Biology","volume":null,"pages":null},"PeriodicalIF":2.2000,"publicationDate":"2022-08-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9475666/pdf/","citationCount":"3","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Integrative Organismal Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/iob/obac038","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2022/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 3
Abstract
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.
尽管在许多脊椎动物(哺乳动物和鱼类)中都进化出了巨大的体型和专性的滤食机制,但间歇性的公羊(弓步)滤食是一种特殊的须鲸家族所特有的:须鲸。弓步进给是一种高成本、高效益的进给机制,它需要整合非定常运动(即加速度和机动);尺度对这种觅食模式的生物力学和能量学的影响仍然是人们深入研究的主题。我们的研究目标是将多传感器标签与无人机镜头相结合,以确定体型等形态计量学对运动学冲刺参数的影响,如吸吸时间、最大冲刺速度和吞噬期间从小须鲸到蓝鲸等一系列物种的减速。我们的研究结果表明,在吃磷虾的情况下,无论大小,动物在有动力和完全没有动力的吞没之间表现出倾斜的梯度,通常在最大的冲刺速度和嘴巴张开时结束。在所有情况下,由尾部产生的少量推进推力都无法克服在吞没过程中经历的高阻力。假设这个推力是最小的,我们就能预测出横冲直撞的最小速度。为了使箭步进食的能量消耗最小化,流体动力学理论预测,无论体型大小,箭步进食速度都会变慢,而下限取决于猎物避免被捕获的能力。我们使用经验数据来验证这一理论,结果发现,即使更高的速度导致更低的觅食效率,最大觅食速度仍然保持恒定且高(约4 m s-1)。无论如何,我们发现体型和觅食效率之间的关系越来越密切,这可以用从猎物身上获得的能量与消耗的能量之比来估计。这一趋势跨越了从一次猛冲到一天的时间尺度,表明大型鲸鱼以更低的成本捕获更多的猎物和更多的能量。