Paleobiology, 23(4), 1997, pp. 482-490 Locomotor evolution in the earliest cetaceans: functional model, modem analogues, and paleontological evidence J. G. M. Thewissen and E E. Fish Abstract.-We discuss a model for the origin of cetacean swimming that is based on hydrodynamic and kinematic data of modem mammalian swimmers. The model suggests that modem otters (Mustelidae: Lutrinae) display several of the locomotor modes that early cetaceans used at different stages in the transition from land to water. We use mustelids and other amphibious mammals to analyze the morphology of the Eocene cetacean Ambulocetus natans, and we conclude that Ambu- locetus may have locomoted by a combination of pelvic paddling and dorsoventral undulations of the tail, and that its locomotor mode in water resembled that of the modem otter Lutra most closely. We also suggest that cetacean locomotion may have resembled that of the freshwater otter Pteronuru at a stage beyond Ambulocetus. 1. G. M. Thewissen. Department qf Anatomy, Northeastern Ohio Universities College of Medicine. Roots- town, Ohio 44242 E E. Fish Department of Biology, West Chester Unrwrsrty. West Chester, Pmnsvlmnia 19380 Accepted. 7 July 1997 Introduction that wen the earliest whales had adopted modem ways of swimming. In spite of noting The locomotor morphology of terrestrial differences in overall morphology and muscle mammals is very different from that of aquatic development, Kellogg (1936) proposed that mammals. The musculoskeletal system of swimming mammals displays conspicuous late Eocene Basilosaurus had a tail fluke and specializations that can be considered as ad- implied that it swam by dorsoventral oscilla- aptations for life in the water. These adapta- tion (p. 286), the locomotor mode of all mod- tions are the result of dramatic morphological em cetaceans. Barnes and Mitchell (1970) re- evolution that has made it impossible for the constructed Basilosaurus with a broad horizon- most specialized secondarily aquatic mam- tal tail fluke, and Uhen (1991) found that ver- mals, cetaceans and sirenians, to locomote on tebral dimensions of Basilosaurus indicated land. that it swam similarly to modem cetaceans. Cetaceans descended from terrestrial mam- Gingerich et al. (1994) concluded that dorso- mals, and their amphibious ancestors must ventral oscillations of the tail were the mode have had morphologies consistent with land of locomotion for the protocetid cetacean Rod- i and aquatic-locomotion. Both ancestors (land hocetus kasrani. mammals) and descendants (marine cetace- One of the few cetaceans for which a differ- ans) of these amphibious taxa must have been ent means of aquatic locomotion has been pro- morphologically very different from these posed is Ambulocetus nntans, an Eocene ceta- amphibious whale intermediates. The terres- cean from Pakistan (Thewissen et al. 1994, trial relatives of cetaceans, mesonychians, did 1996). Most of the limb skeleton of this taxon not resemble early cetaceans in their locomo- is known and is very different in shape from tor morphology. The postcranial skeleton of that of all other known cetaceans. On the basis mesonychians shows that they were cursors to of overall morphology, Thewissen et al. (1994, varying degrees (Zhou et al. 1992; O'Leary 1996) concluded that the power stroke of Am- and Rose 1995). bulocetus during swimming resulted mainly In spite of the locomotor changes that early from strokes of the feet, and not from strokes cetaceans underwent, few authors in the pa- of the tail. Propulsive strokes were probably in leontological literature have analyzed these the dorsoventral plane, similar to modem ce- changes, and it has commonly been assumed taceans. 0 1997 The Paleontological Society. All rights reserved. 0094-8373/97/230e0006/$1.00 'I LOCOMOTION IN THE EARLIEST CETACEANS 483 In contrast to the paleontological literature, guild. If the model is valid, members of these the zoological literature has extensively ad- guilds can be used as functional analogues for dressed changing function of aquatic loco- the stages of cetacean swimming. Among the motion in early cetacean evolution. Howell three terminal locomotor stages, the sequence (1930 p. 21) discussed the evolving locomotor leading to cetaceans can best be studied using patterns in aquatic mammals and stated that modem analogues, because a variety of mod- “there seems to be a decided tendency for em mammals of diverse phylogenetic back- aquatic mammals to develop as the primary ground are members of each guild. means of locomotion a single organ or pair of This paper will modify Fish’s (1996) model organs.” Howell (1930) also made a distinc- and develop a morphological context for the tion between (modem) cetaceans with a fusi- part of the model that relates to cetacean ori- form body and those with an anguiliform gins (Fig. 1). We here propose morphological body (such as Basilosmtrtcs), and suggested correlates for the different locomotor stages that the latter type swam differently. SIijper and test these with the use of quantitative and (1946) studied spinal morphology of cetace- qualitative morphological data from the skel- ans and concluded that Eocene cetaceans and eton. Although the morphology of mammali- mysticetes used undulating locomotor pat- an swimmers has been extensively studied terns, whereas odontocetes employed more (e.g., Howell 1930; Slijper 19361, there has been oscillating patterns, but he did not base these very little explicit work relating morphology conclusions on observations of actual swim- to swimming modes. ming cetaceans. The model as discussed here differs from Locomotor patterns in semiaquatic and that of Fish (1996) in two important respects. aquatic mammals have been studied in mus- We do not differentiate between the two pelvic telid carnivores (Tarasoff et al. 1972; Williams paddling modes, as these are not distinct mor- 1983, 1989; Fish 1994), the rodent Ondatrn phologically. On the other hand, we do distin- (Fish 1982a,b, 1984), dideiphid marsupials guish two distinct modes of dorsoventral un- (Fish 1993a), talpid moles (Hickman 1984), dulation, one that is propelled by the feet (pel- and delphinid cetaceans (Slijper 1961; Fish vic undulation, as discussed by Fish, 1996) and Hui 1991; Fish 1993c). These analyses are and one that is driven by the tail (caudal un- based on kinematic data of swimming behav- dulation). ior and on hydrodynamic principles. They Once the morphological context for the commonly did not involve morphological model is established, we test the model by analyses, the focus of this paper. Williams considering the morphology of one early ce- (1989) and Fish (1993b) discussed the kine- tacean, Ambulocefus nntuns. Ambufocefusis the matics and energetics of several swimming most primitive cetacean for which much of the modes of semiaquatic mammals, and Fish postcranial skeleton is known (Thewissen (1996) put the transition of drag-based to lift- 1994). It is also one of the few archaic cetace- based forms of aquatic locomotion in an evo- ans for which most of the limb skeleton is lutionary perspective. Fish’s (1996) model known. If cetacean locomotor evolution summarized the evolution of the three most- passed through the stages identified in Fig. 1 derived modes of aquatic locomotion in mam- and if Ambulocefus is a good model for the an- mals (lateral pelvic oscillation in phocid seals, cestor of modem cetaceans, Ambulocetus must pectoral oscillation in otariid sea lions, and have displayed a locomotor pattern that is dorsoventral caudal oscillation in cetaceans). typical for one of these stages, and a modern According to this model, cetacean locomotion mammal could be a locomotor analogue for went through the following stages: quadru- Ambulucetus. Thewissen et al. (1994) did not pedal paddling, alternate pelvic paddling, si- identify a modem mammal as a locomotor an- multaneous pelvic paddling, dorsoventral un- alogue of Ambulocefus, instead noting that its dulation, and caudal oscillation. Each of these locomotor pattern combined aspects of seals, locomotor modes is used by a number of mod- otters, and cetaceans. Thewissen et al. (1996) em mammals that compose a locomotor proposed that Ambulocefus’s swimming w?s . 484 J. G.M. THEWISSEN AND F. E. FISH 1936; Fish 1982a,b, 1984). Terrestrial moles (Sculopus, Tulpu) swim by paddling with all four feet, but the more aquatic star-nosed mole, Condyluru, abandons this gait for pelvic paddling during fast swimming (Hickman 1984). Lutru cunudensis swims using a variety of paddling modes (including quadrupedal and forelimb-only), but during rectilinear surface FIGURE 1. Model for the locomotor stages that cetace- swimming it usually paddles by alternating ans passed through in their evolution, modified from a strokes of the hind limbs (Fish 1994). Fore- model developed by Fish (1996). Whereas Fish's model distinguished two pelvic paddling stages, we recognize limbs are not involved in locomotion during only one on the basis of morphological attributes. Fish this locomotor pattern. The locomotor cycle specified the "dorsoventral undulation" mode based on for each limb can be divided into a power the locomotor behavior of Enhydra, but we distinguish "pelvic undulation" and "caudal undulation," and pro- stroke and a recovery stroke. During the for- pose that the swimming mode of Enhydro (pelvic un- mer, the hip is extended (distal femur moves dulation) may not have been a necessary intermediate caudally), the knee is extended, and the heel for the origin of cetacean locomotion. Clades of modem mammals with locomotor behaviors in these categories is plantarflexed while the foot is splayed out. are also listed. The opposite motions occur in the recovery stroke, where the surface area of the foot is re- duced by half to minimize drag (Fish 1984). A most similar to that of Enhydra. Fish (1996) similar sequence occurs in Chirunectes: the toes used data on Enhydra from Williams (1989) to are abducted and extended throughout the characterize his dorsoventral undulation power stroke and propulsive force is provided stage. However, Enhydra is a pelvic undulator by extension at the hip and by knee extension and we propose below that cetacean ancestors (Fish 1993a).