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Cenozoic Mammalian Heubivoues Fuom the Ameuicas &HQR]RLF0DPPDOLDQ+HUELYRUHVIURPWKH$PHULFDV5HFRQVWUXFWLQJ$QFLHQW'LHWVDQG 7HUUHVWULDO&RPPXQLWLHV $XWKRU V %UXFH-0DF)DGGHQ 6RXUFH$QQXDO5HYLHZRI(FRORJ\DQG6\VWHPDWLFV9RO SS 3XEOLVKHGE\Annual Reviews 6WDEOH85/http://www.jstor.org/stable/221724 . $FFHVVHG Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=annrevs. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology and Systematics. http://www.jstor.org Annu. Rev. Ecol. Syst. 2000. 31:33-59 Copyright? 2000 by Annual Reviews. All rights reserved CENOZOICMAMMALIAN HERBIVORES FROM THE AMERICAS:Reconstructing Ancient Diets and TerrestrialCommunities BruceJ. MacFadden Florida Museumof Natural History, Universityof Florida, Gainesville, Florida 32611; e-mail: [email protected] Key Words browsers,grazers, isotopes, teeth, morphology, paleoclimate * Abstract Herbivoryfirst evolved in terrestrialmammals during the late Cre- taceous, -100 million years ago (Mya). Of the -35 ordinal-levelclades of extinct or extanteutherian mammals from the New World, -24 have been adaptedto her- bivoryin one formor another.Dental adaptations for specializedterrestrial browsing are firstrecognized during the early Cenozoic (Paleocene-Eocene).Mammalian her- bivoresadapted for grazingdid not become widespreadin the New Worlduntil the middleCenozoic; it seems thatthis adaptationand the spreadof grasslandsoccurred duringthe late Oligocene(30 Mya) in SouthAmerica 10 million yearsearlier than in NorthAmerica (20 Mya).Carbon isotopic evidence from fossil herbivoreteeth indi- catesthat C3 plantspredominated until the late Miocene (8 Mya).Thereafter, C3 and C4 terrestrialcommunities diversified. Late Pleistocene extinctions 10,000 yearsago decimatedthe diversity of mammalianherbivores, particularly those of largerbody size. INTRODUCTION As primaryconsumers of plantbiomass, herbivores represent the majorityof diver- sity in ancientmammalian radiations. The fossil recordof mammalianherbivores in North and South Americais relativelywell representedover the past 65 million years (My). During this time therehave been considerablechanges in climate and plantdiversity that affected the structureand distributionof mammalianherbivore communities.In the past severaldecades, some importantfactors have influenced our understandingof, and our ability to reconstruct,ancient mammalian herbivore communities.Paleontological discoveries continuously improve our knowledge of the fossil recordand oftentimesfill in critical gaps. New techniques,such as anal- yses of stable isotopes and enamel microwear,have advancedour ability to make paleodietaryinterpretations. Continuous refinements in dating techniquesallow a better understandingof the time sequence of mammalianherbivore community evolution. 0066-4162/00/1120-0033$14.00 33 34 MACFADDEN The fossil recordreveals a time dimension not availableto modem ecologists. Paleontologistscan track discrete communities throughmillions of years during which basic communitystructure is preservedbut new taxa originateand fill eco- logical niches vacatedby taxa thatbecame extinct. This is called a chronofauna,a term originallyproposed by Olson (64,65). This paperreviews the fossil recordof terrestrialmammalian herbivore commu- nities overthe past 65 my, the Cenozoic Erain Northand SouthAmerica. Whenever possible, emphasisis placed on recentdiscoveries and new techniquesthat enhance understandingof this subject. The Cenozoic was a time of great global change, and it is somewhatartificial to devote this review to the New World,when parallel faunal changes occurredin the Old World.However, this focus is determinedby the availablespace; the interestedreader can also consult previousreviews on this general subject (31, 36, 94, 95). BACKGROUNDAND METHODS In 1873, the Russian paleontologist Kowalevsky published a classic paper (38) describing fossil horses from Europe. He asserted that the evolution of horses with short-crownedteeth to those with high-crownedteeth during the Miocene indicated a correspondingchange in diet from browsing to grazing. Since that time, the tooth crown height of fossil herbivoreshas been used to interpretthe diets of ancient mammals (Figure 1). Within the past few decades, other tech- niques have addedindependent evidence to an understandingof ancientherbivore diets. Complementinggross tooth morphology,studies of skull morphology,and enamelmicrowear, stable carbon isotopes now can be used to reconstructCenozoic herbivorecommunities. Morphology Modern herbivorousmammals with short-crowned(brachyodont) teeth, e.g., the tapir(Tapirus) or deer (Odocoileus), are generallyadapted to feeding on soft, leafy vegetation and hence are browsers. In contrast, modem herbivorousmammals with high-crownedteeth, e.g., the zebra (Equus) and bison (Bison), are generally grazers.High-crowned is defined as unwornpremolar or molar teeth in which the height exceeds the occlusal length of the tooth (Figure2A). High-crownedteeth are either of finite growth,like those of horses, or ever-growing(hypselodont) during the animal'slifetime, like those of some grazingrodents. The adaptivesignificance of high-crownedteeth is, in most cases, related to the abundanceof phytoliths in grasses. Phytoliths are microscopicbodies of silica (SiO2, the same compoundas glass) within grasses that tend to wear teeth down and are an adaptationof the plant against herbivory(59). There are, however, some exceptions to this general short-crownedbrowser/high-crowned grazer pattern. For example, short-crowned llamas (Lama)are principally grazers (29, 52), whereassome extincthigh-crowned CENOZOICMAMMALIAN HERBIVORES 35 * Pulp cavity B [ Bone H Enamel Cementum ,1,. Figure 1 Comparison of short-crowned(brachyodont) human tooth (a) versus high- crowned horse tooth (b) showing expansion of the crown relative to the root area. From Ref. 33 and reproducedwith permissionof CambridgeUniversity Press. horses were principallybrowsers (53). Nevertheless, tooth morphology serves as a general model to interpretextinct herbivorediets. There also is a correlationbetween high-crownedteeth and open-countryhabi- tats. Thus, some high-crownedherbivores may incorporateconsiderable amounts of grit into their diets from dust on the plant foods that they eat close to the land surface (29). Terrestrialgrazers are generally considered to include animals that feed predominantly(>90%) on grasses (29), althougha species is also a grazerif it crops plants other than grasses (e.g., forbs) that form the low ground cover in some biomes. Certaincranial characters are also highly correlatedto diet in extantherbivorous mammals.For example, the muzzle shape and incisor width of modem ungulates distinguish browsers from grazers (Figure 2). Grazerstend to have more trans- versely straight muzzles and incisors of generally similar size, which together form a functionalcropping mechanism to procuregrass and other plants near the ground surface. In contrast,browsers have more rounded muzzles and differen- tiated incisors, which togetherform a cropping mechanism for selective feeding from trees and shrubs(32, 84). These differencesare also apparentin fossil herbi- vores, e.g., Oligocene notoungulatesin SouthAmerica (78) andMiocene sympatric horse species in North America (47). Othercharacters, like the depth of the jaw, developmentof the bony masseterprominence on the cheek, and position of the orbit, also indicate browsing versus grazing diets (85). 36 MACFADDEN A B il LEN M~3EN ilLEN i3LEN UMAPL E N cc: cc: MUZWDTH CJAWA~~~~prsnt)~~(present) ~~" LEWAGL (absent) Figure 2 Dental and skull charactersused to assess browsingversus grazing. (A) crown height, or hypsodontyindex (HI) is the ratioof unworncrown height (UCRNHT)to molar anteroposterior length (UMAPL); in this case the HI is -2.6, indicating a grazer. (B) Relative incisor lengths (ilLEN and i3LEN) and muzzle width (MUZWDTH)indicate a browser(narrow, left) or a grazer (broad, right). (C) The position of the orbit (ORBITPOS),presence or absence of the masseter prominence(MASSPROM), and depthand posterior angle of thejaw (JAWDEPTH,JAWANGLE) indicatea browser(left) or a grazer(right). Modified from Ref. 52 andreproduced with permission of the PaleontologicalSociety. The mastication of various foodstuffs imparts distinctive microscopic wear patterns to the tooth enamel of modem herbivorous mamnmalswith known diets (83,86). Using modem analogs, extinct herbivore diets can be interpreted using dental microwear. These enamel-microwear
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