Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size

Abstract

Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations.

Swimming kinematics and efficiency of entangled North Atlantic right whales

“…Combining average η p for this right whale (Eg 3911) with losses due to muscle activity (η m = 0.25) leads to an η a of 0.05 and 0.04 and maximum overall efficiencies of 0.13 and 0.13 for descent and ascent, respectively (Table 4), supporting the conservative 0.15 efficiency factor used in previous studies (Goldbogen et al 2011, Potvin et al 2012, van der Hoop et al 2014b). η i was significantly lower when entangled; although this does not represent the realized case, it illustrates a simpler estimate (based on C T alone) and that the optimal performance of the system is affected by these different entanglement conditions.…”

“…η a = η p × η m . Some previous studies (Goldbogen et al 2011, Potvin et al 2012 sum the total losses of 0.75 and 0.10 to obtain η a = 0.15, instead of multiplying (0.25 × 0.90 = 0.225), though 0.15 represents a conservative estimate.…”

Novel muscle and connective tissue design enables high extensibility and controls engulfment volume in lunge-feeding rorqual whales

“…In this model, for any lunge comprising engulfment through a complete mouth opening and closing cycle, the engulfed water mass must also be rapidly set into forward motion, a function attributed in the passive model to elastic loading and unloading of the VGB (Orton and Brodie, 1987;Simon et al, 2012). However, recent unsteady hydro-mechanical models of this process suggest that the highly compliant nature of the VGB would require all the water collected in the fully expanded ventral cavity (posterior to the temporal mandibular joint; Fig.1) to be rapidly accelerated to the same speed as the whale once the elastic limit of the VGB was reached, thus requiring very large VGB extensions to provide the high forces needed (Potvin et al, 2009;Potvin et al, 2012). Furthermore, it was determined that engulfment by passive VGB inflation would result in drag forces too low to decelerate the whale as quickly as was observed in direct field measurements (Goldbogen et al, 2006).…”

Increased proximity of vessels reduces feeding opportunities of blue whales in the St. Lawrence Estuary, Canada

“…Blue whales employ a relatively costly foraging strategy called lunge feeding (Acevedo-Gutiérrez et al 2002. This foraging tactic might lead to shorter than expected dive times (Croll et al 2001) and regular exhaustion of oxygen stores, placing additional constraints on surface recovery time (Potvin et al 2012). In St. Lawrence Estuary blue whales, optimal dive time and theoretical aerobic dive limit (TADL) converge with increasing depth, because for deeper dives (generally during daytime) a greater amount of time is spent travelling through the water column, thereby constricting time and oxygen stores left available for foraging at depth (Doniol-Valcroze et al 2011).…”