LOCOMOTOR ADAPTATIONS IN THE LIMB SKELETONS OF NORTH AMERICAN MUSTELIDS by Thor Holmes A Thesis Presented to The Faculty of Humboldt State University In Partial Fulfillment of the Requirements for the Degree Master of Arts June, 1980 LOCOMOTOR ADAPTATIONS IN THE LIMB SKELETONS OF NORTH AMERICAN MUSTELIDS Approved by the Master's Thesis Committee Chairman Approved by the Graduate Dean TABLE OF CONTENTS Page Acknowledgments iv Abstract vi Introduction 1 Materials and Methods 11 Results and Discussion 30 Intraspecific Variation 30 Species Comparisons 46 Forelimb 46 Hindlimb 68 Conclusions 91 Literature Cited 97 Appendices 105 ACKNOWLEDGMENTS This study was partially funded by a thesis grant from the Biology Graduate Student Association at HSU. I thank the following museums and their curators for the use of materials in their collections: American Museum of Natural History; California Academy of Science; Carnegie Museum of Natural History; Field Museum of Natural History; Humboldt State University, Museum of Vertebrate Zoology; University of Kansas Natural History Museum; Los Angeles County Museum of Natural History; Museum of Zoology, University of California, Berkeley; Michigan State University, The Museum; National Museum of Natural History; San Diego Museum of Natural History; San Diego Natural History Museum; University of California at Los Angeles; University of Michigan Zoology Museum; University of Montana Department of Zoology; University of Puget Sound, Museum of Natural History; I would like to thank particularly Murray Johnson, Helen Kafka, and Shiela Kortlucke for help during the times I used their collections. Suzanne Edwards, Judy Fessenden, Cynthia Hofmann, Rebecca Leuck, Bob Sullivan, my brother, Thomas, and my wife, Elaine helped me make measurements. Mike Gwilliam, Tim Lawlor, Steve Smith, and Bob Sullivan helped me with computer programs. Cynthia Hofmann, Elaine Holmes, and Kathy McCutcheon helped type the manuscript. Kathy typed the final draft. V I would like to thank the members of my committee, Jake Houck, Frank Kilmer, Tim Lawlor, John Sawyer, and Jim Waters for time they invested in my thesis and my education. I would like to thank particularly my major professor, Tim Lawlor, for help, friendship, encouragement, and sundry other contributions to my life and my education far too numerous to mention here. Finally I wish to thank Elaine, my wife, for a decade of support in every sense of the word. And I wish to acknowledge that she, more than any other person, is the reason that I can look back from this point in my life and smile. ABSTRACT The morphology and proportions of the limb skeletons of thirteen species of North American mustelids are examined. A series of forty-nine ratios is generated for each species. Ratios are analyzed using standard descriptive statistics; mean, standard deviation, variance, standard error, coefficient of variation, and range. Ratios are also analyzed with a closest connection (Prim) network. Qualitative comparisons of appendicular skeletons are made with drawings of each limb element. Progressive specialization from an hypothesized primitive condition to fossorial, arboreal-cursorial, aquatic, and ambulatory modes of locomotion is revealed in limb skeletons of the Mustelidae. Relationships between morphology and proportions of mustelid limb skeletons, and modes of locomotion are discussed. INTRODUCTION The family Mustelidae, comprising twenty-five recent and some seventy fossil genera (Anderson and Jones, 1967), is one of the most diverse families of carnivores. Only its ecological counterpart in the Old World tropics, the family Viverridae, contains more extant genera. Mustelids range in size from small (35 g) to medium (37 kg). They are distributed throughout the world except for Australasia and Antarctica. The Mustelidae apparently arose from the most ancient carnivorans, family Miacidae, about 35 mybp. The origin of the Mustelidae within the miacids seems to be separate from that of the other canoid carnivores. They quickly adopted the typical mustelid specializations of a strongly carnivor- ous dentition, short powerful jaws, prominent pre- and post- glenoid processes, and a long cylindrical body (Ewer, 1973; Romer, 1966). Mustelids as a group also are characterized by a weak zygoma. Ewer (1973) and Gambaryan (1974) suggested that the weak zygoma and a long cylindrical body are adaptations to hunting small mammals within their burrows, a method of predation that still characterizes the largest and one of the most primitive living genera, Mustela (Table 1). Despite specializations of cranial and axial osteology the mustelids retain a very generalized limb structure. They do, however, show fusion of two carpals, the scaphoid 2 Table 1. -- Earliest record for ten genera of the family Mustelidae (after Romer, 1966). Genus Time of Probable Origin Mustela Upper Miocene Martes Middle Miocene Eira Pleistocene Gulo Pleistocene Spilogale Lower Pleistocene Mephitis Pleistocene Conepatus Upper Pliocene Taxidea Upper Pliocene Lutra Lower Pliocene Enhydra Pleistocene PLEISTOCENE Mephitis Eira Gulo Enhydra Spilogale Conepatus Taxidea PLIOCENE Lutra Mustela MIOCENE Martes 3 and lunar. They also have lost a third carpal, the centrale. These are interpreted as cursorial specializations and are the common heritage of all carnivores (Ewer, 1973; Vaughn, 1978). Mustelids are plantigrade to digitigrade. The extent to which they are digitigrade is never as pronounced as in the Felidae or Canidae. The mustelids are pentadactyl and all of the digits touch the substrate. Members of the family retain relatively short, stocky limbs and do not have retractile claws. Gambaryan (1974) suggested that the basic cursorial gait in the Mustelidae, the bound or half bound, is a result of their long narrow body. Variations on the basic gait include a slow ambulatory walk (Mephitis, Conepatus), a speedy trot (Taxidea, Mustela), and a bear-like shuffle (Gulo). The Mustelidae, at least as regards appendicular anatomy, more closely resemble basal fissipeds than any extant group of carnivores. While a generalized limb skeleton characterizes most mustelids, some species have evolved ambulatory, arboreal, semi-aquatic, aquatic, and fossorial habits. Mustelids, therefore, present the student an opportunity to observe a spectrum of locomotor adapta- tions in a single family. There are numerous studies on locomotor specialists. Horses, gazelles, cheetahs, whales, and moles have all been examined. Studies of this kind are valuable in that they reveal the types of adaptations to specific modes of 4 locomotion that typify specialists. I have chosen, however, to examine the array of locomotor adaptations that charac- terize the Mustelidae. No mustelid is highly specialized for a particular mode of locomotion. For that reason I think that an investigation of the Mustelidae is of particular interest because it promises to elucidate locomotor trends in types of animals often ignored in the locomotor literature. Some recent members of the Mustelidae have been the object of considerable osteological or myological study (Fisher, 1942; Howard, 1973, 1975; Leach, 1977a, 1977b; Leach and Dagg, 1976; Ondrias, 1960, 1961; Tarasoff, 1972). As yet no one has studied the entire spectrum of locomotor adaptations in the Mustelidae either myologically or osteo- logically. Some studies on the limb skeletons of other families of carnivores have been made: Hildebrand (1952, 1954), on canids; Goynea and Ashworth (1975) and Hopwood (1947), on fends; and Taylor (1970, 1974, 1976), on viverrids. Techniques used in those studies could produc- tively be applied to the Mustelidae. The burgeoning literature on primate locomotion (Ashton et al., 1971; Ashton and Oxnard, 1964; Jenkins, 1976; Lewis, 1972; Reisenfeld, 1974) contains techniques with possible applica- tions to mustelids. A similar, if somewhat older, literature on locomotion in mammals in general (Brown and Yalden, 1973, and citations therein) provides a valuable backdrop against which to compare mustelids. Finally there are studies of 5 the effect of modes of life on the skeleton, or on particular skeletal elements (Chapman, 1919; Jones, 1953; Lehmann, 1963; Taylor, 1914; Yalden, 1972). These papers are especially useful in that they elucidated the type of morphological indicators that suggest specializations to a particular mode of life. The taxonomic position of some mustelids is not well understood (Simpson, 1945), but the family lends itself to separation into four locomotor categories corresponding roughly to the four main recognized subfamilies (Fig.1 ). The Mustelinae are weasel-like forms which typically have sub-cursorial, scampering habits. This is the oldest and most primitive subfamily. Martens, fishers, and tayras, the larger members of this group, have arboreal proclivities. The mink, another member of the Mustelinae, is amphibious. The Mephitinae, the skunks, are ambulatory. The Melinae include most of the badgers; they are fossorial. Finally, the Lutrinae comprises the most aquatic fissipeds, the otters. The American badger, Taxidea, and the wolverine, Gulo, are the subject of some taxonomic debate. Nevertheless, they may be conveniently grouped with the badger and weasel subfamilies, respectively, in regard to locomotion. North American mustelids encompass all of the locomotor types that characterize the family as a whole. Hence they should constitute a representative subset of the range of locomotor specializations that characterize mustelids as a whole.