Sink or swim? Bone density as a mechanism for buoyancy control in early cetaceans

Abstract

Previous analyses have shown that secondarily aquatic tetrapods, including whales, exhibit osteological adaptations to life in water as part of their complex buoyancy control systems. These structural specializations of bone span hyperostosis through osteoporosis. The past 15 years of paleontological effort has provided an unprecedented opportunity to examine the osteological transformation of whales as they make their transition to an obligate aquatic lifestyle over a 10-million-year period. It is hypothesized that whales manifest their osteological specialization in the same manner as extant semiaquatic and fully aquatic mammals. This study presents and analysis of the microstructural features of bone in early and late archaic cetaceans, and in a comparative sample of modern terrestrial, semiaquatic, and aquatic mammals. Bone histology was examined from the ribs of 10 fossilized individuals representing five early cetacean families, including Pakicetidae, Ambulocetidae, Protocetidae, Remintonocetidae, and Basilosauridae. Comparisons were then made with rib histology from nine genera of extant mammals including: Odocoileus (deer), Bos (cow), Equus (horse), Canis (dog), Lutra (river otter), Enhydra (sea otter), Choeropsis (pygmy hippo), Trichechus (sea cow), and Delphinus (dolphin). Results show that the transition from terrestrial, to semiaquatic, to obligate aquatic locomotion in archaeocetes involved a radical shift in bone function achieved by means of profound changes at the microstructural level. A surprising finding was that microstructural change predates gross anatomical shift in archaeocetes associated with swimming. Histological analysis shows that high bone density is an aquatic specialization that provides static buoyancy control (ballast) for animals living in shallow water, while low bone density is associated with dynamic buoyancy control for animals living in deep water. Thus, there was a shift from the typical terrestrial form, to osteopetrosis and pachyosteosclerosis, and then to osteoporosis in the first quarter of cetacean evolutionary history. Anat Rec 290: 638-653, 2007 Key words: bone; histology; microstructure; osteopetrosis; pachyo steosclerosis; osteosclerosis; osteoporosis; cetacean; archaeocete; fossil; whale; aquatic; rib; anatomy Mammals and reptiles that secondarily invade aquatic niches typically undergo remarkable structural transformations related to the mechanical constraints of locomotion in water versus land. Although the most obvious skeletal changes occur at the gross anatomic level, equally dramatic modifications occur in the structural properties of bone tissue, ranging across extremely high to extremely low density (for a review of literature, see

“Pachyostosis” in aquatic amniotes: a review

“…should not be considered semi-aquatic but fully aquatic forms. Recent histological analyses realized on the most primitive Cetacea (Madar 2007;Gray et al 2007) and on the raoellid Indohyus have revealed the presence of pachyostosis s.l. (Thewissen et al 2007).…”

A new skeleton of the cryptoclidid plesiosaurTatenectes laramiensisreveals a novel body shape among plesiosaurs

“…When added to the bone mass of the girdle elements, Tatenectes had a significant mass of heavy bone concentrated ventrally and medially in the thorax. This is unusual given that pachyostotic bone is more evenly distributed in most taxa possessing it (Domning and de Buffr ´ enil, 1991;Gray et al, 2007), including the one other known pachyostotic plesiosaur (Pachycostasaurus dawni: Cruickshank et al, 1996). One other consideration is relevant, and that is the placement of the lungs within the body cavity.…”

“…Pachyostosis in general is a method of passive buoyancy control (de Buffr´ enil et al, 1990;de Ricql` es and de Buffr ´ enil, 2001), and its presence is generally correlated with life in shallow water (Gray et al, 2007). Pachyostosis in the skeleton of secondarily marine tetrapods seldom occurs in fast swimming, highly maneuverable taxa (Taylor, 2000), or in habitually deep-water forms (Gray et al, 2007). The added mass of pachyostotic bones acts as ballast to help the animal resist the dragging or buffeting effects of the turbulent environment at or near the water surface (de Ricql ` es and de Buffr ´ enil, 2001).…”

The origin and early evolution of whales: macroevolution documented on the Indian Subcontinent

“…The largest pakicetids were similar in size to a wolf, and it is not likely that these waters were suffi ciently deep for pakicetids to swim. Just like Indohyus, pakicetids also had osteosclerotic limb bones suggesting that these whales were waders, not swimmers (Grey et al 2007). Pakicetid fossils are approximately 50 million years old, although it is likely that the family had a longer temporal range.…”