Comparative feeding kinematics and performance of odontocetes: belugas, Pacific white-sided dolphins and long-finned pilot whales

Abstract

SUMMARYCetaceans are thought to display a diversity of feeding modes that are often described as convergent with other more basal aquatic vertebrates (i.e. actinopterygians). However, the biomechanics of feeding in cetaceans has been relatively ignored by functional biologists. This study investigated the feeding behavior, kinematics and pressure generation of three odontocetes with varying feeding modes (belugas, Delphinapterus leucas; Pacific white-sided dolphins, Lagenorhynchus obliquidens; and longfinned pilot whales, Globicephala melas). Four feeding phases were recognized in all odontocetes: (I) preparatory, (II) jaw opening, (III) gular depression, and (IV) jaw closing. Belugas relied on a feeding mode that was composed of discrete ram and suction components. Pacific white-sided dolphins fed using ram, with some suction for compensation or manipulation of prey. Pilot whales were kinematically similar to belugas but relied on a combination of ram and suction that was less discrete than belugas. Belugas were able to purse the anterior lips to occlude lateral gape and form a small, circular anterior aperture that is convergent with feeding behaviors observed in more basal vertebrates. Suction generation in odontocetes is a function of hyolingual displacement and rapid jaw opening, and is likely to be significantly enhanced by lip pursing behaviors. Some degree of subambient pressure was measured in all species, with belugas reaching 126kPa. Functional variations of suction generation during feeding demonstrate a wider diversity of feeding behaviors in odontocetes than previously thought. However, odontocete suction generation is convergent with that of more basal aquatic vertebrates.

Suction feeding preceded filtering in baleen whale evolution

“…Nevertheless, the anterior, posterior and labial wear of the individual teeth is consistent with water and abrasive particles being forcibly expelled from the oral cavity through the diastemata. Similar water expulsion behaviour following suction has been observed in living species, such as pilot whales, belugas, leopard seals and Australian fur seals (Hocking et al, 2013;Hocking et al, 2014;Kane and Marshall, 2009;Werth, 2000a). During water expulsion, the jaws would likely have been held slightly open, causing the nearly occluding, interdigitating tooth rows to form a series of small gaps defined by the rims of the individual diastemata and the tips of the occluding upper or lower teeth.…”

“…It is one of a limited number of fossil whales documenting the transition from raptorial to filter feeding; its cranial morphology disputes prior conjecture about the widespread presence of baleen in aetiocetids; and it provides the first reported evidence of suction feeding at the pivotal mysticete transition towards filter feeding and giant size. The ability to generate suction is fundamental to most marine vertebrates, and widespread among extant marine mammals, including pinnipeds and cetaceans (Hocking et al, 2013;Hocking et al, 2014;Kane and Marshall, 2009;Werth, 2000b;Werth, 2006). Nevertheless, up to this point it has rarely been associated with mysticete evolution, other than in reference to the highly unusual mammalodontids (Fitzgerald, 2010;Fitzgerald, 2012).…”

“…Archaic mysticetes, including aetiocetids, likely inherited both a functional dentition and the ability to use suction for intraoral transport from their archaeocete ancestors (Werth, 2000b). Water ingested as a result of suction was expelled prior to swallowing (Hocking et al, 2013;Hocking et al, 2014;Kane and Marshall, 2009;Werth, 2000a), with the prey either being physically held in place, or the teeth, jaws and surrounding soft tissues acting as a barrier, or simple sieve, retaining food items inside the mouth (Bloodworth and Marshall, 2005;Hocking et al, 2013). Some of these early whales, including NMV P252567, Mammalodon and the ancestor of modern mysticetes, honed their suction capabilities to the point where they became able to capture prey, and we suggest that it was this transition, not filter feeding, that ultimately initiated tooth loss in the chaeomysticete lineage.…”

Feeding kinematics and performance of basal otariid pinnipeds, Steller sea lions (Eumetopias jubatus), and northern fur seals (Callorhinus ursinus): implications for the evolution of mammalian feeding

“…These kinematic variables were selected to determine the behavioral repertoire of prey capture, and characterize the feeding mode of Steller sea lions and northern fur seals. They were also selected to test the hypothesis that rapid jaw opening (GAOV) contributes to subambient pressure generation, and build upon our comparative feeding performance dataset for marine mammals (following Bloodworth and Marshall, 2005;Marshall et al, 2008Marshall et al, , 2014aKane and Marshall, 2009).…”

Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newtIchthyosaura alpestris(Salamandridae)

“…Most aquatic vertebrates use a hydrodynamic mechanism, which typically includes a fast oropharyngeal volume expansion by means of abduction of the jaws and hyobranchial elements. This generates a suction flow into the expanding mouth, which draws the prey and its surrounding water into the oral cavity (Muller and Osse, 1984;van Leeuwen and Muller, 1984;Lauder, 1985;Lauder and Shaffer, 1986;Van Damme and Aerts, 1997;Lemell et al, 2002;Marshall et al, 2008;Kane and Marshall, 2009;Heiss et al, 2013). However, as suction feeding does not work on land because of the low density and viscosity of air, most terrestrial vertebrates have evolved a highly modified capture mode where precise contact of the prey by the jaws and/or tongue plays a central role (Larsen and Guthrie, 1975;Bramble and Wake, 1985;Dockx and De Vree, 1986;Findeis and Bemis, 1990;Schwenk, 2000;Herrel et al, 2012).…”