Energetic tradeoffs at extreme body size
Keywords: Biology.

Large body size is energetically expensive and physiologically challenging, requiring large-bodied animals to employ a suite of adaptations to maintain a positive energy balance and perform all the necessary functions for life. Rorqual whales (Balaenopteridae), as some of the most massive animals to ever live, are an ideal group to study why large body size evolved and how it is maintained on the individual level. This group has a simple fusiform body shape like many other fast-moving marine species, suggesting that physical rules governing drag reduction and propulsive efficiency in smaller animals are scale-dependent across wide body size ranges. Alternately, the rorqual foraging apparatus and high-speed lunge-feeding behavior are unique within the animal kingdom, allowing them to engulf vast quantities of prey in an energetically efficient manner. The combination of these adaptations reduces costs and increases energetic intake beyond what is seen in other large-bodied animals, resulting in rorquals not only being able to maintain their extreme body size, but also develop a capital breeding strategy whereby they forage for a portion of the year and rely on those energy stores throughout some of the longest migrations ever seen. For the first time, a combination of new technologies has allowed me to study the scaling laws governing large body size in rorqual whales in high-resolution across a range of body sizes and species. In Chapter 1, I focus on the scale-dependence of simple locomotor parameters such as oscillatory frequency and swimming speed. These variables have long been studied in comparative biomechanics but remain poorly understood for animals at the upper extremes of body size. I combined morphometrics from aerial UAV photogrammetry, whale-borne inertial sensing tag data, and hydrodynamic modeling to study the locomotion of five rorqual species. I 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. My 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 as predicted by hydrodynamic theory for high locomotor performance while minimizing energy use. In Chapter 2, I built upon our previous results and continued to use data from whale-borne inertial sensors coupled with morphometric measurements from aerial UAVs to calculate the hydrodynamic performance of oscillatory swimming in six baleen whale species ranging in body length from 5-25m. I found that mass-specific thrust increases with both swimming speed and body size. Froude efficiency, defined as the ratio of useful power output to the rate of energy input (Sloop, 1978), generally increased with swimming speed but decreased on average with increasing body size. This finding is contrary to previous results in smaller animals where Froude efficiency increased with body size. However, Froude efficiency remained generally high (> 90%) in all rorqual species. In Chapter 3, I investigated the unique behaviors related to lunge feeding in rorqual whales. 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. I used a combination of multi-sensor tags paired with UAS footage to determine the impact of morphometrics (i.e., 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. My 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 propulsive thrust generated by the tail was 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. I 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 energetic economy. Regardless, I found an increasing relationship between body size and energetic economy, estimated as the ratio of energetic gain from prey to energetic cost of the lunge. 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. In Chapter 4, I combined energetic estimates from earlier analyses of swimming and foraging to determine the energetics of rorqual whales' extreme migrations under various conditions. For a successful foraging season, the energetic cost of migration relative to seasonal food intake only amounts to ~20% across body sizes, while a poor foraging year could result in relatively exorbitant migratory costs of ~100% or more. I also found that migratory costs are dependent on total distance, duration, and swimming speed. Combining a theoretical model with satellite tracks of individual whales, I determined that longer migrations are more costly and occur at higher speeds than shorter migrations. In a rapidly changing ocean, even small differences in the distance or duration of a migration could have major impacts on individual fitness. My conclusion describes how the major findings of this dissertation relate to energy balance and life history for the largest animals to ever evolve