Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whalesBalaenoptera physalus

Abstract

Lunge-feeding in rorqual whales represents the largest biomechanical event on Earth and one of the most extreme feeding methods among aquatic vertebrates. By accelerating to high speeds and by opening their mouth to large gape angles, these whales generate the water pressure required to expand their mouth around a large volume of prey-laden water. Such large influx is facilitated by highly extensible ventral groove blubber (VGB) associated with the walls of the throat (buccal cavity). Based on the mechanical properties of this tissue, previous studies have assumed lunge-feeding to be an entirely passive process, where the flow-induced pressure driving the expansion of the VGB is met with little resistance. Such compliant engulfment would be facilitated by the compliant properties of the VGB that have been measured on dead specimens. However, adjoining the ventral blubber are several layers of well-developed muscle embedded with mechanoreceptors, thereby suggesting a capability to gauge the magnitude of engulfed water and use eccentric muscle action to control the flux of water into the mouth. An unsteady hydrodynamic model of fin whale lunge-feeding is presented here to test whether engulfment is exclusively passive and compliant or involves muscle action. The model is based on the explicit simulation of the engulfed water as it interacts with the buccal cavity walls of the whale, under different heuristically motivated cavity forces. Our results, together with their comparison with velocity data collected in the field, suggest that adult rorquals actively push engulfed water forward from the very onset of mouth opening in order to successfully complete a lunge. Interestingly, such an action involves a reflux of the engulfed mass rather than the oft-assumed rebound, which would occur mainly at the very end of a lunge sequence dominated by compliant engulfment. Given the great mass of the engulfed water, reflux creation adds a significant source of hydrodynamic drag to the lunge process, but with the benefit of helping to circumvent the problem of removing prey from baleen by enhancing the efficiency of cross-flow filtration after mouth closing. Reflux management for a successful lunge will therefore demand wellcoordinated muscular actions of the tail, mouth and ventral cavity.

Discovery of a sensory organ that coordinates lunge feeding in rorqual whales

“…Histological, anatomical and kinematic evidence indicate that this sensory organ responds to both the dynamic rotation of the jaws during mouth opening and closure, and ventral groove blubber 7 expansion through direct mechanical linkage with the y-shaped fibrocartilage structure. Along with vibrissae on the chin 9 , providing tactile prey sensation, this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment, a paradigm that is consistent with unsteady hydrodynamic models and tag data from lunge-feeding rorquals [10][11][12][13] . Despite the antiquity of unfused jaws in baleen whales since the late Oligocene 14 ( 23-28 million years ago), this organ represents an evolutionary novelty for rorquals, based on its absence in all other lineages of extant baleen whales.…”

“…Dynamic pressure imposed on the floor of the mouth forces inversion of the tongue 18 and expansion of the ventral groove blubber (VGB) to accommodate the engulfed water 5,7 . Hydromechanical models suggest that the expansion of the oropharyngeal cavity (or ventral pouch 8 ) requires active resistance, in a highly coordinated fashion, by eccentric action from musculature associated with the VGB [10][11][12][13] . The lunge sequence ends once the mandibles close around the volume of engulfed water, with the VGB and the oropharyngeal cavity slowly returning to its original size, allowing the baleen plates to filter the captured prey from the engulfed water 3 .…”

“…The mandibular symphysis has a direct mechanical linkage to the VGB 7 through the y-shaped fibrocartilage (YSF) structure 8 , which has a raised stem that emerges from the symphysis and extends posteriorly in two branches, parallel to the jaws and embedded within the VGB 8 . How these structures are integrated into the engulfment apparatus has remained enigmatic, although hydro-mechanical models and kinematic data from tagged rorquals suggest that lunge feeding is a highly coordinated process [10][11][12][13] . Here, we identify a novel sensory organ that is mechanically linked to both bony and soft tissues, and can provide the brain with mechanosensory information for coordinating the rapid and marked expansion of the oral cavity during a lunge.…”

Convergent Evolution Driven by Similar Feeding Mechanics in Balaenopterid Whales and Pelicans

“…Additionally, these extensible tissues contain an intermediate muscle layer. In rorquals, this muscle layer serves to limit the rate of buccal cavity expansion by accelerating the engulfed water forwards (Potvin et al, 2009). We speculate that the muscle layer may play a similar role in pelicans during engulfment feeding.…”

“…An open mouth moving at high speed underwater generates considerable pressure drag, the same phenomenon that provides resistance to moving an open bag under water (Goldbogen et al, 2007). Additionally, rorquals actively accelerate water in their buccal cavities after a lunge-feeding event, giving rise to ''engulfment drag'' (Potvin et al, 2009). In both rorquals and pelicans, the elastic floor of the mouth is attached to the ventral surface of the mandibles along their length; therefore, the combined drag forces generated during a feeding event should exert a dorsoventrally oriented bending force distributed along the mandibles, rostral to the craniomandibular joint (Field et al, 2010).…”