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Miocene Ungulates and Terrestrial Primary Productivity: Where Have All the Browsers Gone?

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Miocene Ungulates and Terrestrial Primary Productivity: Where Have All the Browsers Gone? Miocene ungulates and terrestrial primary productivity: Where have all the browsers gone? Christine M. Janis*†, John Damuth‡, and Jessica M. Theodor* *Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912; and ‡Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106 Edited by David Pilbeam, Harvard University, Cambridge, MA, and approved May 5, 2000 (received for review March 21, 2000) Progressive changes are observed in both the composition of Mammalian faunal composition has the potential for provid- mammal faunas and vegetation during the Miocene epoch [24–5 ing information about vegetation structure and productivity that mega-annum (Ma)]. These changes are usually interpreted as a is not readily available from paleobotanical data. Fossil floras response to climatic changes. In the traditional view, forests or provide taxonomic information, from which general vegetation woodlands gradually gave way to more open habitats, with types can often be inferred. However, within vegetation types, grazing (grass-eating) ungulate (hoofed) mammal species replac- paleobotany provides little direct evidence for absolute abun- ing the browsing (leafy-vegetation-eating) species as grasslands dances of plant life forms or for productivity. Moreover, plant expanded. However, data from fossil assemblages in the Great macrofossils are seldom preserved in the same habitats as fossil Plains region of North America show that this faunal change was vertebrates (5, 6). not a one-for-one replacement of browsers by grazers, as usually We present data on community composition in Miocene thought. Typical late early Miocene (17 Ma) fossil communities faunas of the Great Plains region of North America and included extraordinarily high numbers of browsing ungulate spe- analyze trends in the percentage and absolute number of cies, comprising a fauna that cannot be directly analogized with species of different dietary types. The results suggest that the any present-day community. Both maximum species richness of all decline of browsing species was more extreme than previously ungulates and the proportion of browsers declined steadily in recognized and also document the unique features of the ungulate communities through the middle Miocene, to levels faunas of the early Miocene when the decline began. These comparable to those of the present by the late Miocene. The faunas have no analog under any present-day regime of rainfall resulting dramatic, cumulative loss of browsing species constitutes and temperatures and thus carry a signal about early Miocene one of the strongest faunal signals of the late Tertiary (but was not environmental conditions that has hitherto been unrecog- a single ‘‘event’’). We suggest that the early Miocene browser-rich nized. The detailed pattern of the loss of browsing species from communities may reflect higher levels of primary productivity in North American ungulate communities may indicate changing Miocene vegetation, compared with equivalent present-day veg- levels of primary productivity in terrestrial ecosystems. This etation types. The observed decline in species richness may rep- evolutionary pattern, in turn, may have implications both for resent a gradual decline in primary productivity, which would be the history of atmospheric CO2 levels and for explanations for ͞ consistent with one current hypothesis of a mid-Miocene decrease the C3 C4 transition at 7 Ma. in atmospheric CO2 concentrations from higher mid-Cenozoic values. Methods Faunal Data. Data on continent-wide generic diversity were based volution of plant and animal communities in mid to high on new compilations from the most recently published synthesis Elatitudes over the past 50 myr (a unit of one million years as (13). Data on species co-occurrence and community composi- a simple quantity of time) is marked by a general reduction in the tion were assembled from the primary literature and from extent of forest and woodland ecosystems and, from around 15 examination of museum collections (Table 1). Taxonomy follows mega-annum (Ma), the spread of grasslands (1–4). This biotic ref. 13, and the time scale and dates follow ref. 14. We chose shift has long been attributed to increases in higher latitude localities that contained a good sample of ungulate taxa and also aridity and temperature seasonality (5, 6). represented a single, and likely attritional, faunal sample (e.g., a Mammal faunas changed over this time span in response to single quarry). Each time period is represented by three local- these environmental trends (7–9). Ungulates (hoofed, herbivo- ities, with the exception of 9 Ma, 7.5 Ma, and 4.0 Ma (two rous mammals such as horses, rhinos, deer, antelope, cattle, pigs, localities each) and 15 Ma (four localities). The oldest faunas camels, elephants, etc.) are sensitive to the quality and quantity sampled are latest early Miocene, from the late Hemingfordian of their forage and exhibit a range of dietary specializations, Land Mammal ‘‘age,’’ corresponding to the inception of the from feeding purely on grass (grazers) to feeding almost entirely ‘‘Clarendonian chronofauna.’’ This chronofauna represents a on leaves of dicotyledonous plants (browsers). The received view period of relative ecosystem stability between 17.5 and 8.8 Ma, is that, as habitats became more open and grasslands expanded, coinciding with the domain of the North American Miocene grazing species simply replaced browsing species, much as one would observe today passing along a broad geographic transect from wetter to drier habitats. In this scenario, the decline in This paper was submitted directly (Track II) to the PNAS office. numbers of browsers and the eventual extinction of many Abbreviations: Ma, mega-annum, a unit of one million years before the present in the lineages are often perceived as the inevitable fates of more radioisotopic time scale. primitive herbivores, with their place in the ecosystem being †To whom reprint requests should be addressed at: Department of Ecology and Evolution- ary Biology, Box G-B207, Brown University, Providence, RI 02912. E-mail: Christine_Janis@ taken by better-adapted grazers. Significant changes in mammal brown.edu. faunas are also thought to have accompanied the transition at 7 The publication costs of this article were defrayed in part by page charge payment. This EVOLUTION Ma to grasslands dominated by plant species that used the C4 article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. photosynthetic pathway (10–12). §1734 solely to indicate this fact. PNAS ͉ July 5, 2000 ͉ vol. 97 ͉ no. 14 ͉ 7899–7904 Downloaded by guest on September 29, 2021 Table 1. Fossil faunas of the Great Plains region of North America used in this study. Fauna LMA Ma B SM M H T Bellville Fm., White Rock LF, KS L. Bl. 2.0 1 0 2 3 6 Kiem Fm., Sand Draw LF, NB L. Bl. 2.0 1 0 2 4 7 Long Pine Fm., Big Springs LF, NB L. Bl. 2.0 2 0 4 3 9 Broadwater Fm., Broadwater LF, NB E. Bl. 3.0 1 0 2 3 6 Deer Park Fm., Deer Park LF, KS E. Bl. 3.0 1 0 1 4 6 Rexroad Fm., Rexroad LF, KS E. Bl. 3.0 4 0 1 4 9 Ash Hollow Fm., Santee LF, NB L’est Hp. 4.0 2 2 2 4 10 Ash Hollow Fm., Devil’s Nest Airstrip LF, NB L’est Hp. 4.0 4 2 2 5 13 Ash Hollow Fm., Honey Creek, NB L. Hp. 5.5 1 1 2 4 8 Ogallala Fm., Edson Quarry LF, KS L. Hp. 5.5 3 2 3 5 13 Ash Hollow Fm., Mailbox LF, NB L. Hp. 5.5 2 2 2 5 11 Ash Hollow Fm., Minium Quarry, KS L.E. Hp. 6.5 2 1 3 5 11 Ogallala Group, Wray LF, CO L.E. Hp. 6.5 3 1 2 7 13 Ash Hollow Fm., Cambridge FT 40 LF, NB L.E. Hp. 6.5 4 2 3 7 16 Snake Creek Fm., Aphelops Draw LF, NB E.E. Hp. 7.5 2 2 3 4 11 Ash Hollow Fm., Lemoyne Quarry, NB E.E. Hp. 7.5 3 2 4 5 14 Snake Creek Fm., Snake Creek LF, NB L. Cl. 9.0 4 4 2 6 16 Ash Hollow Fm., Blue Jay Quarry, NB L. Cl. 9.0 3 3 3 5 14 Ogallala Fm., Wakeeny Creek LF, KS E. Cl. 10.0 2 2 2 4 10 Ash Hollow Fm., Big Spring Canyon LF, SD E. Cl. 10.0 3 3 4 7 17 Ash Hollow Fm., Little Beaver B Quarry, NB E. Cl. 10.0 5 4 6 5 20 Ash Hollow Fm., Trail Creek Quarry LF, NB L. Ba. 12.0 2 2 5 2 11 Valentine Fm., Myers Farm, NB L. Ba. 12.0 9 4 3 2 18 Ogallala Fm., Kennesaw LF, CO L. Ba. 12.0 4 2 3 2 11 Valentine Fm., Carrot Top Quarry, NB M. Ba. 13.5 6 3 4 3 16 Pawnee Creek Fm., Horse & Mastodon Quarry, CO M. Ba. 13.5 2 2 4 2 10 Valentine Fm., Norden Bridge Quarry, NB M. Ba. 13.5 14 5 7 3 29 Olcott Fm., Humbug Quarry, NB E. Ba. 15.0 9 4 11 0 24 Olcott Fm., Echo Quarry, NB E. Ba. 15.0 10 5 10 0 25 Pawnee Creek Fm., Eubanks LF, CO E. Ba. 15.0 7 2 3 0 12 Sand Canyon Beds, Observation Quarry, NB E. Ba. 15.0 13 3 0 0 16 Sheep Creek Fm., Thompson Quarry, NB L. Hf. 17.0 10 3 12 0 25 Box Butte Fm., Foley Quarry, NB L. Hf. 17.0 8 1 4 0 13 Sheep Creek Fm. equiv., Ginn Quarry, NB L. Hf. 17.0 8 2 3 0 13 Running Water Fm., Aletomeryx Quarry, NB E.
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