Skeletal Adaptations

From small, probably terrestrial, carnivorous or insectivorous Mesozoic ancestors, mammals have diversified to occupy almost every major environment throughout the world. They have evolved a remarkable diversity of skeletal adaptations for life in the air, in trees, on land, under ground, and in water. Due in part to the versatile tribosphenic molar, mammalian dentitions have become modified for almost every conceivable diet, including leaves, grass, roots and tubers, seeds, fruits, sap, nectar, bark, meat, fish, mol-lusks, krill, insects and other invertebrates, and even bones.

Some mammals have relatively generalized teeth that can handle a diet of mixed plant and animal items; they are omnivores.

The generalized anatomy described in the preceding section is often modified in similar ways in different clades, in association with similar diets, habitats, and lifeways. This tendency leads to the phenomena of convergence and parallelism—the independent acquisition of similar morphology in distantly related and closely related organisms, respectively. The resulting resemblances are known as ho-moplasy. Here I review some of the characteristics of the dentition and skeleton in mammals adapted for different lifestyles.

The dentitions of many extant insectivores, like those of primitive Paleogene mammals, are relatively little changed from those of their Cretaceous ancestors. They have sec-odont teeth with high, sharp cusps, often joined by sharp, bladelike crests. Their incisors are often enlarged and procumbent, and the trigonids of the lower molars tend to be much higher, and commonly larger, than the talonids. Both the ectoloph of the upper molars and the occluding lower molar crests may be arranged in the form of a W a condition termed dilambdodont (e.g., shrews and moles; Fig. 2.16A). Dilambdodonty promotes more efficient cutting (Butler, 1996) and also occurs in some herbivorous lineages (see Fig. 2.3F). In some insectivores (e.g., golden moles, tenrecs, Solenodon) the upper molar paracone and metacone are connate (closely appressed and joined at the base) and set well in from the buccal margin, so the ectoloph forms a V-shape, and the protocone is reduced; this configuration is

Mesonychids Pachyaena
Fig. 2.10. Mammalian carpus and manus, exemplified by Eocene Pachyaena. Roman numerals indicate metacarpals. Key: cen, centrale; cun, cuneiform; lun, lunate; mag, magnum; pis, pisiform; sc, scaphoid; td, trapezoid; tm, trapezium; unc, unciform. (From Rose and O'Leary, 1995.)

described as zalambdodont. Zalambdodonty, or a close approximation to it, occurs in various noninsectivoran clades as well. In highly zalambdodont forms, the metacone may be lost and the paracone may be near the center of the tooth; the lower molars tend to have very tall trigonids and greatly reduced talonids (Fig. 2.16B). The paracone occludes in the notch between trigonid and talonid (called the hypo-

flexid), and shearing occurs predominantly between the anterior crest of the upper molar (preparacrista) and the back of the trigonid (protocristid; Asher et al., 2002). Bats and some small primates, such as tarsiers, also have insectivorous dentitions.

Myrmecophagous mammals, which specialize on a diet of ants and termites, include members of several orders. The most extreme forms (echidna, anteaters, and pangolins) have lost all the teeth and have shallow, delicate mandibles. Those that retain teeth (numbat, some armadillos, aardvark, and aardwolf; Fig. 2.16E) tend to have small, homodont teeth, sometimes reduced in number and lacking enamel, but some have more than the usual number of simple teeth. The skull is often elongate and tubular, in association with a long, protrusile tongue. Many myrmecophagous mammals have evolved fossorial skeletons (see below) that enable them to tear into ant and termite nests.

Carnivorous (meat-eating) mammals typically have small incisors, large canines, and one or more pairs of upper and lower cheek teeth specialized into cutting blades called car-nassials (Fig. 2.16C). In Carnivora the carnassials are P4 and M1, but other teeth are modified into carnassials in the extinct Creodonta. The most strictly carnivorous forms, such as cats, are termed hypercarnivores. They have long, sharp carnassial blades and have reduced or lost the molars behind the carnassials. Some carnivorans have evolved away from the original carnivorous diet of their ancestors. Omnivorous and frugivorous carnivorans, such as bears, raccoons, and palm civets, have broad, bunodont teeth and lack specialized carnassials. Carnivores tend to have well-developed tempo-ralis muscles. Consequently, the skull generally has a prominent sagittal crest (reduced in frugivorous forms), and the coronoid process of the dentary is large. The mandibular condyle is situated at about the level of the toothrow, which maximizes power at the carnassials.

Certain specialized faunivorous diets are associated with particularly unusual dentitions. (Faunivorous is a general term for a diet consisting of animals of any kind.) Piscivorous (fish-eating) mammals, such as seals and dolphins, often have simple, homodont, conical teeth, in some cases greatly exceeding the normal number. Walruses and some seals and otters (Carnivora) eat mollusks and sea urchins, using teeth that are either peglike or broad and flat, for crushing hard objects. Mysticete whales, which filter-feed on plankton, have lost the teeth and replaced them with keratinous, straining baleen plates suspended from the maxilla.

Herbivores (plant-eating mammals, including ungulates and some rodents and primates) can usually be recognized by their broad grinding molars, and (in ungulates) a tendency toward molariform premolars. Beyond these general similarities, however, herbivores have achieved considerable dental diversity. They may be brachydont or hypsodont. Some are bunodont, but more often their molariform teeth have multiple shearing crests; lophodonty or selenodonty is common. The incisors of herbivores often form a cropping apparatus that is separated from the cheek teeth by a gap, or diastema. In some forms the upper incisors are absent

Ungual Phalanges Rheas
Fig. 2.11. Ungual phalanges of some Eocene and extant mammals in lateral and dorsal views. Compare with Fig. 2.17. Scale bars = 5 mm. (From Rose, 1990.)

and the lowers work against a corneous pad covering the premaxilla. The enamel of specialized herbivores shows complex infolding with dentine windows and cementum.

There are several specialized kinds of herbivory. Frugivores (herbivores that feed primarily on fruit; e.g., fruit bats, some monkeys and apes, kinkajou) tend to have brachy-

dont, bunodont teeth, with minimal development of shearing crests. As noted above, frugivorous carnivorans lost their shearing teeth through evolution. Some small marsupials and primates feed on tree gum and sap, for which they have evolved large, procumbent incisors used to gouge through bark. As might be expected, their molars are generally very low crowned, with indistinct surface features. Nectivorous forms (nectar and pollen feeders), including certain bats and marsupials, also reduce the cheek teeth, in the most extreme case to just a few vestigial pegs (the honey possum, Tarsipes).

Folivores are herbivores specialized for feeding on leaves. They typically have lophodont or bilophodont (with two transverse ridges) cheek teeth. Examples include tapirs, langurs and colobus monkeys, and the koala. In some folivores the enamel is crenulated and multiple shearing blades are present (Fig. 2.16D). As a result of their heritage, tree sloths and their extinct relatives differ from other folivores in having simple cylindrical teeth. The most specialized folivores are grazers. Grazers have evolved various mechanisms to cope with a diet of grass, which contains a high component of abrasive silica phytoliths. Commonly the teeth of grazers are hypsodont, with multiple lophs (selenodont, as in ruminant artiodactyls) or complex enamel patterns (as in horses; Fig. 2.16F). In the most specialized forms the cheek teeth grow continuously throughout most of the life of the animal.

The skulls of more specialized herbivores are often elongate, to accommodate molarized premolars. Ungulate skulls are often adorned with horns, antlers, or bony protuberances. The herbivore mandible is deep in back, with a large angular process where the well-developed masseter and medial pterygoid muscles attach. The latter, particularly, are related to transverse movement of the jaw during chewing, which is especially important in herbivores. In contrast to

Ungulate Skeletal Adaptations
Fig. 2.12. Mammalian pelvis (innominate) and sacrum, exemplified by late Eocene Patriomanis. (Modified from Rose and Emry, 1993.)
Diacodexis

Fig. 2.13. Left femur and tibia of some extant and Eocene mammals. Distal view of femur at top. The complete fibula is shown only in the three genera on the left; the distal fibula is indicated for Diacodexis. Tupaia is scansorial, Erinaceus is generalized terrestrial, Rhynchocyon is cursorial, Diacodexis and Hyracotherium were cursorial, Palaeanodon was fossorial, Viverra is generalized terrestrial, and Paradoxurus is arboreal. Dagger (f) indicates an extinct Eocene taxon. Scale bars = 1 cm.

Fig. 2.13. Left femur and tibia of some extant and Eocene mammals. Distal view of femur at top. The complete fibula is shown only in the three genera on the left; the distal fibula is indicated for Diacodexis. Tupaia is scansorial, Erinaceus is generalized terrestrial, Rhynchocyon is cursorial, Diacodexis and Hyracotherium were cursorial, Palaeanodon was fossorial, Viverra is generalized terrestrial, and Paradoxurus is arboreal. Dagger (f) indicates an extinct Eocene taxon. Scale bars = 1 cm.

Hyracotherium
Fig. 2.14. Feet of Eocene mammals: (A) Oxyaena, generalized terrestrial; (B) Chriacus, arboreal; (C) Phenacodus, incipiently cursorial; (D) Diacodexis, cursorial/ saltatorial; (E) Hyracotherium, cursorial. Scale bars = 1 cm. (Modified from Rose, 1990.)

Fig. 2.15. Right astragali of some extant and Eocene mammals. Distal view of the astragalar head is shown for the first four genera. Dagger (f) indicates an extinct Eocene taxon. Left scale bars = 1 mm; right scale bars = 5 mm.

Dasypus Choloepus Manis Palaeanodon1 Phenacodusf Hyracotheriumf Bunophorusf Chriacus*

Fig. 2.15. Right astragali of some extant and Eocene mammals. Distal view of the astragalar head is shown for the first four genera. Dagger (f) indicates an extinct Eocene taxon. Left scale bars = 1 mm; right scale bars = 5 mm.

Adaptations MammalsHyracotherium Teeth

Fig. 2.16. Some specialized mammalian dentitions: (A) dilambdodont and insectivorous (Nesophontes); (B) zalambdodont (Solenodon); (C) hyper-carnivorous (Dinictis); (D) dilambdodont and folivorous/frugivorous (Cynocephalus); (E) myrmecophagous (Stegotherium); (F) hypsodont grazer (Equus), skull and crown view of upper teeth. (A-B from McDowell, 1958; C from Matthew, 1910b; D from MacPhee et al., 1989; E from Scott, 1903-1904; F from Gregory, 1951.)

Age Mammals
Fig. 2.17. Ungual phalanx shape in various behavioral guilds based on eigenshape analysis of extant mammals. At right are the mean lateral and dorsal profiles of each locomotor group. (From MacLeod and Rose, 1993.)

the situation in carnivores, the coronoid process is typically reduced, and the mandibular condyle is positioned well above the toothrow in herbivores.

The postcranial skeletons of mammals also have distinctive modifications that reflect their habitat, locomotion, or lifestyle. Particularly useful accounts of the skeletal characteristics of different locomotor groups can be found in Gambaryan (1974), Hildebrand et al. (1985), Van Valken-burgh (1987), and Hildebrand (1995). The primitive mammalian skeleton, from which more specialized skeletal adaptations evolved, was presumably a rather generalized one that enabled progression on uneven substrates and was, therefore, conducive to both terrestrial and arboreal environments. In part, this versatility resulted because most basal mammals were very small, and for them there was probably little difference between the varied substrates of the forest floor and those of brush, vines, tree trunks, and branches (Jenkins, 1974). Climbing was therefore very likely part of their locomotor repertoire. However, some of the most ancient mammals for which skeletons are known were already specialized for particular lifestyles, hence the primitive state for mammals remains uncertain. Among living mammals, several locomotor categories are recognized, which also reflect habitat (see, e.g., Eisenberg, 1981).

Many living mammals are adept climbers and spend considerable time in the trees. Those that forage and shelter in trees are considered arboreal, whereas able climbers that also spend much of their time on the ground are scansor-ial. Mammals in both of these categories have similar skeletal specializations for maximizing mobility at the shoulder, elbow, wrist, hip, and ankle, although these modifications tend to be more extreme in arboreal forms (Figs. 2.7, 2.13, 2.14). They can rotate the radius to supinate the forearm. The manus and pes are typically plantigrade (with palms and soles in contact with the substrate) and adapted for grasping, often with abducted or opposable pollex and hallux. Some specialized arboreal mammals—including sciurids and procyonids—have evolved anatomical modifications that allow them to hyperinvert or "reverse" the hind feet, thus enabling them to descend from trees headfirst or to hang upside down (Jenkins and McClearn, 1984). The digits of most arboreal mammals bear sharp, curved, laterally flattened claws (formed of keratin), which are supported by bony ungual phalanges of similar shape (Fig. 2.17). In arboreal primates and hyracoids, however, the unguals bear nails. The tail of arboreal mammals is usually long and may be prehensile.

Many primates, carnivores, xenarthrans, and marsupials are arboreal or scansorial. Some highly arboreal mammals (e.g., dermopterans, phalangers, flying squirrels) have evolved a skin membrane, or patagium, which enables them to glide between tree branches. These glissant forms tend to have delicate, elongate limb elements and specializations in the manus and pes associated with attachment and control of the patagium. In bats, the only volant (flying) mammals, the forelimbs are modified to support active wings. The skeleton is very lightly built and delicate. The forelimb bones in particular are very long and slender, with elongate digits that support the wing membrane. Mobility at the shoulder, elbow, and wrist is greatly restricted. The hind limbs are small and very thin.

Terrestrial mammals spend most or all of their time on the ground. Although some are able, if infrequent, climbers, others are incapable of climbing trees. Generalized terrestrial mammals (e.g., hedgehogs, tenrecs, civets, some bears) lack clear modifications for specific locomotor specializations. They may show some restriction of mobility at limb joints, but not to the extent seen in cursorial forms. Their foot posture ranges from plantigrade to digitigrade (supported by the digits, with palm and heel off the ground). The claws are usually longer, not as curved, and broader ventrally than in scansorial or arboreal forms.

There are several specialized categories of terrestrial mammals, described in this and the following paragraphs. Cursorial mammals are adapted for running, and their skeletons show modifications that increase stride length and rate, which results in greater speed (Hildebrand, 1995). They have elongate limbs, with the intermediate and distal segments especially long and slender (Figs. 2.13, 2.14). Muscle masses tend to be concentrated in the proximal part of the limb to reduce the weight of the distal portion. The limb joints are modified to restrict motion to a parasagittal plane. The bony crests and processes for muscle attachment tend to be reduced compared to those of climbers and diggers, and are situated closer to the joints they affect, an adaptation for speed. The clavicle is usually absent, and the ulna and the fibula are often reduced or fused to the radius and tibia, respectively Runners usually have long to very long metapodials, the lateral ones sometimes reduced or lost. Fusion of some of the carpals or tarsals is common. Hoofs are often present. When claws are retained, the terminal phalanges supporting them are longer, less curved, and broader than in climbing mammals (Fig. 2.17). The stance of cursors is typically either digitigrade (standing on the digits, with the metapodials raised off the ground, as in various carnivores) or unguligrade (standing on the terminal phalanx or hoof, as in most ungulates).

Saltatorial mammals are specialized for jumping, and are usually propelled by the hind limbs (e.g., rabbits). The skeleton generally resembles that of cursors, with similar limitations on joint mobility, but the hind limbs are usually much longer than the forelimbs (see, e.g., Fig. 9.4). When the hind limbs are used together for bipedal jumping, as in kangaroos, jerboas, and kangaroo rats, the gait is called ricochetal. The intermembral index ([length of humerus + radius] / [length of femur + tibia] x 100) of ricochetal mammals is less than 50, compared to an average index of 75 in generalized mammals (Howell, 1944). The tibia and fibula are usually fused at one end or both ends for stability, and the metatarsals may be exceptionally long. Some bounding mammals have fused cervical vertebrae to provide neck stability. Such primates as tarsiers, galagos, and some lemurs are arboreal saltators.

Very heavy terrestrial mammals are described as gravi-portal (with limbs adapted for supporting heavy weight; see Figs. 7.25, 12.29B, 13.12, 13.23). Most graviportal mammals are large ungulates (e.g., elephant, hippopotamus, rhinoceros) and, therefore, presumably evolved from somewhat cursorial antecedents. They stand with straight, columnar limbs, an adaptation to minimize the stresses imposed on the limb bones. Unlike typical cursors, the intermediate limb segments (radius and tibia) are shorter than the proximal segments. The manus and pes have robust, spreading digits with short, broad phalanges and hoof-bearing unguals.

Mammals adapted for digging are fossorial (e.g., golden moles, armadillos, badgers, pocket-gophers, various squirrels, other rodents). The most specialized fossorial mammals (moles, marsupial mole) are subterranean, seeking food and shelter underground and rarely coming to the surface. The term "fossorial" is sometimes restricted to just these subterranean dwellers, the term "semi-fossorial" being used for diggers that live above ground. In this text the broader usage is applied. Fossorial mammals typically have robust skeletons with strong limb girdles and short, heavily built limb bones (particularly the forelimb) that have prominent crests and processes for muscle attachment (Figs. 2.7, 2.13). The ulnar olecranon process tends to be very prominent and long, but the functional length of the intermediate segment of the forelimb is much less than that of the proximal segment. The elements of the manus are short and stout, except for the claws (especially of the middle digit), which may be greatly enlarged. Claws of diggers tend to be longer, shallower, less curved, and ventrally wider than those of climbers (MacLeod and Rose, 1993). Fossorial mammals that also use the head and teeth for digging have a wedge-shaped skull, with a broad lambdoid crest for attachment of neck muscles. In some diggers several cervical vertebrae are fused. The tail is generally reduced in subterranean forms.

Terrestrial mammals adapted for swimming (e.g., otters, beavers, muskrats, capybaras) are termed semi-aquatic. Their limb bones are usually short and stout, with prominent crests and processes for muscle attachment, similar to those of fossorial mammals. The humerus may have a slightly S-shaped profile. Manus and pes tend to have short, spreading digits, which are often webbed. The tail may be long and muscular, and the hind limbs are often specialized for propulsion.

Some mammals have become more committed to life in the water, and are described as aquatic or natatorial (swimming). Most aquatic mammals are marine, but some frequent freshwater. The body of aquatic mammals is often long and streamlined. The neck is commonly very short, and cervical vertebrae may be fused. The forelimbs are short and modified into paddles or flippers with elongate digits, and, in whales, extra phalanges. The hind limbs may be modified like the forelimbs (as in seals), reduced, or vestigial (as in manatees, whales, and dolphins). Limb joint mobility is often severely restricted.

The anatomical adaptations described in the preceding paragraphs have known functional associations in extant mammals. Applying this knowledge to fossils enables educated inferences on the lifeways of extinct mammals.

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Responses

  • anastasio
    How are terrestrial mammals adapted to their environment?
    6 years ago
  • jeanne thurman
    What features in molars and premolars crabeater seal enable filter feed?
    5 years ago
  • sarah
    Why the cervical vertebrae are often fused in digging and swimming mammals?
    4 months ago

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