Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation

Abstract

Foraging methods vary considerably among semiaquatic and fully aquatic mammals. Semiaquatic animals often find food in water yet consume it on land, but as truly obligate aquatic mammals, cetaceans (whales, dolphins, and porpoises) must acquire and ingest food underwater. It is hypothesized that differences in foraging methods are reflected in cetacean hyolingual apparatus anatomy. This study compares the musculoskeletal anatomy of the hyolingual apparatus in 91 cetacean specimens, including 8 mysticetes (baleen whales) in two species and 91 odontocetes (toothed whales) in 11 species. Results reveal specific adaptations for aquatic life. Intrinsic fibers are sparser and extrinsic musculature comprises a significantly greater proportion of the cetacean tongue relative to terrestrial mammals and other aquatic mammals such as pinnipeds and sirenians. Relative sizes and connections of cetacean tongue muscles to the hyoid apparatus relate to differences in feeding methods used by cetaceans, specifically filtering, suction, and raptorial prehension. In odontocetes and eschrichtiids (gray whales), increased tongue musculature and enlarged hyoids allow grasping and/or lingual depression to generate intraoral suction for prey ingestion. In balaenopterids (rorqual whales), loose and flaccid tongues enable great distention of the oral cavity for prey engulfing. In balaenids (right and bowhead whales), large but stiffer tongues direct intraoral water flow for continuous filtration feeding. Balaenid and eschrichtiid (and possibly balaenopterid) mysticete tongues possess vascular retial adaptations for thermoregulation and large amounts of submucosal adipose tissue for nutritional storage. All cetacean tongues also function in prey transport and swallowing. These hyolingual musculoskeletal differences are unique cetacean anatomical adaptations for foraging entirely in an aquatic environment. Anat Rec 290: 546-568, 2007. 2007 Wiley-Liss, Inc.Key words: Cetacea; Mysticeti; Odontoceti; tongue; hyoid; anatomy; histology; feeding; swallowingAlthough tetrapod vertebrates are primarily terrestrial, several lineages have independently and secondarily reverted to a partially or entirely aquatic existence in freshwater and marine habitats, with obvious ecological, behavioral, and morphological consequences. Numerous mammals of various orders inhabit or regularly visit freshwater habitats, but with few exceptions (e.g., the duck-billed platypus, Ornithorhynchus anatinus), and aside from rare differences in diet and foraging behavior, feeding in aquatic monotremes, marsupials, insectivorans, rodents, and ungulates does not differ notably from that of their terrestrial relatives. Such animals may find

Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales

“…If mass-specific metabolic rate decreases with body size, then bulk-filter feeding may represent a mechanism that not only supports large body size (Goldbogen et al 2007), but also allows for the deposition of substantial lipid stores that are required for fasting and long-distance migration (Brodie 1975). Because large amounts of submucosal adipose tissue are present within the tongue in several baleen whale species, the tremendous size of the head may also serve as a compartment for nutritional storage (Werth 2007).…”

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

“…Due to low angular opening velocities observed in pilot whales, this suction capability is likely to be a result of hyolingual depression and not rapid jaw opening. However, hyolingual depression did not differ among belugas, Pacific whitesided dolphins or pilot whales, which reinforces the importance of orofacial morphology to suction generation (Bloodworth and Marshall, 2007;Werth, 2007). Maximum subambient pressure values of pilot whales (23kPa) resembled Pacific white-sided dolphins, and was also less than a harbor porpoise (Kastelein et al, 1997), although kinematics indicated that pilot whales were more similar to belugas in feeding mode.…”

Major taste loss in carnivorous mammals

“…Both animals exhibit an atrophied taste system, exemplified by few taste buds present in their lingual epithelium (21). Consistent with an atrophied taste system, both species exhibit a feeding behavior pattern that suggests that taste may not play a major role in food choice: they swallow their food whole, perhaps minimizing opportunities and needs for taste input (22,23).To further elaborate on the idea that taste behavior, taste receptor function, and feeding ecology are intimately interrelated, we have chosen a comparative approach. Specifically, we have tested two hypotheses.…”

“…Both animals exhibit an atrophied taste system, exemplified by few taste buds present in their lingual epithelium (21). Consistent with an atrophied taste system, both species exhibit a feeding behavior pattern that suggests that taste may not play a major role in food choice: they swallow their food whole, perhaps minimizing opportunities and needs for taste input (22,23).…”