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Dietary plasticity in ungulates: Insight from tooth microwear analysis
Quaternary International 245 (2011) 279e284
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Quaternary International journal homepage: www.elsevier.com/locate/quaint
Dietary plasticity in ungulates: Insight from tooth microwear analysis Florent Rivals a, b, c, *, Gina M. Semprebon d a
ICREA, Barcelona, Spain IPHES, Institut Català de Paleoecologia Humana i Evolució Social, C/ Escorxador s/n, 43003 Tarragona, Spain c Area de Prehistoria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain d Bay Path College, 588 Longmeadow Street, Longmeadow, MA 01106, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 7 August 2010
In recent years, tooth microwear has been used as a powerful tool for investigating mammalian diets in paleontological or archaeological contexts. Tooth microwear techniques were applied to a number of late Pleistocene assemblages of bison (Bison antiquus) from North America to analyze bison dietary traits, but more particularly, to test for dietary plasticity of the fossil species compared to their modern relatives. Modern bison species are known to be grazers from their ecology. However, the results from tooth wear analysis indicate that dietary traits were more diverse in the fossil bison than in their modern relatives. Bison paleodiets range from pure grazing to mixed feeding. The results illustrate not only the dietary plasticity for that species, but also the potential implications involved when using modern species as analogues for reconstructing the ecology of fossil species. Tooth microwear is a good proxy in archaeological contexts because it gives an insight on the diet of the last days of an animal’s life. The intra-population variability in diet is discussed in relation to the duration of formation of the assemblages (natural assemblages versus archaeological Paleo-Indian sites). Ó 2010 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Mammal ecology is frequently investigated through a number of proxies (e.g. locomotion, diet). Insights gained via such proxies are frequently used in paleoenvironmental reconstructions and also for tracking climatic shifts through time (Janis, 1984, 1993, 2003; Vrba, 1988; Aguilar et al., 1999; DeGusta and Vrba, 2005). Morphologic change is one of the most commonly documented responses to ecological changes in the continental fossil record of mammals. Bones and teeth of mammals conveniently preserve important information about two traits e locomotion and diet e both of which play an important role in deciphering the evolutionary history of mammals (Janis, 1984, 2003, 2008). Climatic impact on the evolution of mammals is actually a highly complex phenomenon. It seems reasonable to suppose that both climate change and intrinsic biotic controls would have contributed to faunal evolution, although at different temporal scales and magnitudes. Thus, the response of large mammals to climatic changes is usually synchronous but it may also be asynchronous at times. In the latter case, a discrepancy or time lag may exist between climatic events and changes in mammals. Such * Corresponding author. IPHES, Institut Català de Paleoecologia Humana i Evolució Social, C/ Escorxador s/n, 43003 Tarragona, Spain. Fax: þ34 977 55 95 97. E-mail address: fl[email protected] (F. Rivals). 1040-6182/$ e see front matter Ó 2010 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2010.08.001
a discrepancy may not only result from issues involving differences in time scale and temporal resolution but also may be due to the specific proxy used. For example, changes in skull morphology and tooth wear in the extinct artiodactyl group known as the Dromomerycidae suggested an adjustment in diet during the late Miocene to Pliocene increase in aridity in North America; however, skull morphology apparently lagged behind the apparent dietary shift which was revealed through microwear and mesowear analyses (Semprebon et al., 2004a). Isotope studies reveal that dietary changes may also be more labile than morphologic changes (Feranec, 2007), an insight that may explain the lack of temporal synchronicity between changes in tooth shape and wear (Rivals et al., 2007, 2008; Semprebon and Rivals, 2007, in press; Janis, 2008; Joomun et al., 2008). Similar lags or decoupling between climatic change and various aspects of morphology is very frequently observed in the Pleistocene and Holocene (Kaiser and Franz-Odendaal, 2004; Kaiser and Schulz, 2004; Rivals and Solounias, 2007; Semprebon and Rivals, 2010). It seems evident that speciation events and morphological changes are not necessarily the best ecological proxies, especially when applied to the Quaternary, because morphology (thus speciation) requires many generations for a character to be fixed in a population. In the same way, not all species will exhibit changes in their geographic ranges during periods of climatic change (Blois and Hadly, 2009). Therefore, the biotic response of individuals, species,
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and communities to climatic change is a highly complex phenomenon. Thus, an understanding of more immediate traits, and in particular environments, is an important future research direction and specific procedures such as stable isotopes or dental microwear analyses should be employed to fully understand this phenomenon. Importantly, both tooth microwear and stable isotope analyses are not related to phylogeny, and, therefore, they both reflect the immediate behavior of an animal. In contrast to gross morphology, microscopic tooth wear gives insight into the dietary behavior of the last days or weeks before death, and consequently it provides a snapshot of the environmental condition present at the time the animals were living. Moreover, tooth wear techniques are often preferred over stable isotopes because they are neither destructive nor invasive. This is an important advantage because there are strong destructive sampling policies restricting such work in many collections today. To cope with the decoupling frequently observed between climatic change and various aspects of morphology, tooth microwear analysis is a suitable mechanism for investigating ungulate diets. The diet of extinct ungulates provides valuable information about the food resources available in a given habitat and thus reconstructing paleodiet provides a useful tool for reconstructing paleohabitats. Additionally, information about the diet of extinct ungulates provides insight into resource partitioning and dietary behavior of entire ungulate populations and communities. Consequently, the data can be used to make inferences on differential dietary regimes and seasonal fluctuation in diets. The objective of this paper is to analyze bison dietary traits in the North American late Pleistocene fossil record, and more particularly to evaluate the dietary plasticity of the extinct species in comparison to their modern relatives. A previous study by Rivals et al. (2007) reported geographical differences in diets in four samples of extinct bison. To expand upon that analysis, seven samples of bison (Bison antiquus) from the late Pleistocene of North America were studied (Table 1). The samples come from four States and are identified using the State code followed by a number if several exist for a state: Alaska (AK), Florida (FL), New Mexico (NM1 and NM2), and Texas (TX1, TX2, and TX3). 2. Methodology: tooth wear, a non-destructive proxy for reconstructing diet in fossil ungulates In this study, microscopic analysis of dental wear patterns is used to provide a direct source of evidence for the nature of tooth
use in fossil bison. The microscopic defects on occlusal enamel (microwear) are analyzed here and represent a true snapshot of dietary behavior, sometimes representing the animals’ last meals consumed (last days or week). The high degree of functional similarity in occlusal mechanics for unimodal chewing systems of many herbivorous ungulates provides the prerequisite for an interpretation of microwear patterns as a trophic signal. 2.1. Molding technique Data collection is undertaken using molding and casting techniques. The methodology is adapted from long-standing dental procedural technology. In order to gain high resolution casts, molds are made using fast setting silicone molding materials with low shrinkage. Due to their excellent resolution, such molds can be used for microwear investigation. Making tooth impressions as described does not harm recent or fossil dental tissues because the silicone impression materials used are chemically inert. The method is thus non-destructive. 2.2. Tooth microwear analysis Microwear analysis involves observing the microscopic scars on enamel (Fig. 1) produced by food (phytoliths present in the leaves, grasses, or fruit and seed coats) and grit or dust present on the surface of vegetation. Tooth microwear research originated in the late 1970s using scanning electron microscopes (Rensberger, 1978; Walker et al., 1978) and was later applied to a large variety of taxa. Solounias and Semprebon (2002) proposed a new and greatly simplified methodology for the assessment of the dietary adaptations of living and fossil taxa. This method was developed to allow for microwear scar topography to be accurately analyzed at low magnification (35) using a standard stereomicroscope (Semprebon et al., 2004b). They presented a comparative microwear database of extant artiodactyls, perissodactyls, and proboscideans and interpreted the data to elucidate the diets of these extant ungulates. This database, extended by Semprebon and Rivals, now consists of 76 modern ungulate species. Microwear analysis following the light microscopic protocol by Solounias and Semprebon (2002) was undertaken using a stereomicroscope Zeiss Stemi 2000-C, which has been established as one of the standard forms of equipment for this approach. Microwear is examined on the second enamel band of the paracone of the upper M2 or the protoconid of the lower m2 of adult
Table 1 Description and age of the samples analyzed. Sample locality
Museum curation
Age
Fairbanks area, Alaskaa
Frick Collection at the American Museum of Natural History, New York Frick Collection at the American Museum of Natural History, New York Texas Memorial Museum, Austin, Texas (TMM locality 42345)
Radiocarbon dated to 11,990 135 14C yr B.P. (Stephenson et al., 2001) Rancholabrean North American Land Mammal Age (Webb, 1974) Rancholabrean (late Pleistocene) North American Land Mammal Age (Hester, 1972)
Frick Collection at the American Museum of Natural History, New York
Radiocarbon dated on bone amino acids from different individuals in the bison sample indicating an average age of approximately 10,500 14C yr B.P. (Meltzer et al., 2002) Rancholabrean (late Pleistocene) North American Land Mammal Age (Lundelius, 1972; Otvos and Howat, 1996). Excavated in the 1940’s and yielded the Plainview cultural material which is 10,000 B.P., but most likely late or postFolsom (Holliday, 1985; Holliday et al., 1999; Sellards et al., 1947) Labeled as late Pleistocene in the archives at the AMNH but no other data is available
Seminole field station B, Pinellas County, Florida Blackwater draw locality no. 1, Clovis gravel pit, Curry C., New Mexicob Folsom Quarry, Union County, New Mexico Ingleside fauna, San Patricio County, Texas (TMM locality 30967) Plainview Quarry, Hale County, Texas
Dalhart Sideroad Pit, Hartley County, Texas a b
Texas Memorial Museum, Austin, Texas Texas Memorial Museum, Austin, Texas (TMM locality 725)
Frick Collection at the American Museum of Natural History, New York
Recovered from frozen deposits (Wilkerson, 1932). Contains a stratigraphic sequence with Clovis, Folsom, and other artifacts as well as Rancholabrean faunal remains (Hester, 1972).
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Fig. 1. Occlusal enamel surface of extant (A) and fossil (B) bison teeth at 35. (A) Modern wood bison, Bison bison athabascae (AMNH 86950). (B) Fossil bison, Bison priscus from Folsom Quarry, New Mexico (AMNH 131563).
individuals (young and old adults were discarded). Transparent epoxy casts are examined at 35 magnification using a stereomicroscope using oblique lighting from above the cast. Under the light microscope, pits and scratches are identified and counted within a standard area of 0.16 mm2 on the enamel band following the criteria of Semprebon et al. (2004b). Pits are microwear scars that are circular or sub-circular in outline and thus have approximately similar widths and lengths. Scratches are elongated microfeatures. They are not merely longer than they are wide, but they have straight, parallel sides. Two representative locations are counted because microwear is somewhat variable on a single tooth. The selected second band used here is intermediate in terms of the amount of wear features observed. The number of pits versus scratches for each individual per taxon is recorded. Typical grazers have the highest numbers of scratches and the lowest numbers of pits; typical leaf browsers have lower numbers of scratches and more disparate numbers of pits. Other microwear features are scored with the intent of providing a mechanism to further refine the dietary categorization of ungulates beyond the broad categories of browser versus grazer versus mixed feeder (Solounias and Semprebon, 2002). Table 2 summarizes the microwear variables scored and the type of information that can be gleaned from them.
3. Results A total of 169 teeth of B. antiquus were analyzed. Microwear results are summarized in Table 3. Fig. 2 represents dietary patterns of microwear seen in extant grazers, browsers, and mixed feeders (after Solounias and Semprebon, 2002) and in the extant and fossil bison studied here. The average number of scratches versus the average number of pits per taxon is shown (at 35 magnification). Gray areas delineate extant browsing and grazing scratch/pit morphospaces. It is clear in Fig. 2 that there is no overlap in microwear results between the extant grazing and browsing taxa. Some ungulates, however, are mixed feeders, that is, they switch from browse to grass seasonally or regionally. Consequently, they often fall in the gap between grazers and browsers in terms of average number of scratches but they may have average scratch values that overlap with those of browsers or grazers depending on whether they typically consume relatively more browse or grass.
Because seasonal and regional mixed feeders may have average scratch and pit results that overlap those of browsers and grazers additional calculations are necessary to discriminate them from other trophic groups. While such mixed feeding taxa typically display bimodal scratch distributions when individual raw scratch results are graphed (Solounias and Semprebon, 2002), a simple calculation accords good separation between extant browsers, grazers, and mixed feeders. The percentage of individuals per taxon possessing scratch numbers between 0 and 17 (i.e., the percentage of scratches per taxon that fall in the low-scratch range) offers good dietary resolution of the three main ungulate trophic groups (Semprebon and Rivals, 2007). These low raw scratch percentage results are summarized in Fig. 3 which shows the low-scratch percentage range of scores of extant browsers, grazers, and seasonal/regional mixed feeders as well as the extant and fossil bison studied here. The only overlap that occurs between trophic groups occurs between grazers and seasonal/regional mixed feeders. There is no overlap between the low-scratch ranges of the extant leaf-dominated browsers (72.73e100% of scratches fall
Table 2 Description of typical microwear results for extant ungulates on known diet. Microwear variable
Leaf browsers
Grazers
Mixed feeders
Fruit browsers
Average scratch count Average pit count Large pitsd Raw scratch distribution Puncture pitsd Scratch textured
Low
High
Variable
Variable
Lowa
Low
Variable
High
Low Unimodal elow Absent Fineb
Moderate Unimodal ehigh Absent Coarse or mixed Variablec
Moderate Bimodal (high and low) Absent Coarse or mixedb Variablec
High Variable
Gougingd
Variablec
Present Coarse, mixedb Variablec
Note: scratches that run in a horizontal or oblique direction in relation to the enamel band e i.e., cross-scratches provide information relevant to jaw mechanics and are also noted. a Except in dirty browsing (e.g., camels). b May see hypercoarse scratches in bark consumers (e.g., black rhinoceros) or hard fruit and seed consumers. c Generally higher in taxa encountering grit in foods (e.g., camels, pronghorn, vicuña). d From Solounias and Semprebon (2002).
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Table 3 Microwear summary data for the M2 of fossil and extant bison samples. Sample
Code
N
PIT
SD
SCR
SD
%LP
%CS
%G
SWS
%0e17
Diet
Fossil bison Fairbanks Area, Alaska Blackwater Draw, Clovis Pit, NM Folsom Quarry, New Mexico Seminole Field Station B, Florida Ingleside, Texas Plainview Quarry, Texas Dalhart Sideroad Pit, Texas
AK NM1 NM2 FL TX1 TX2 TX3
27 26 12 13 15 62 14
11.4 17.3 10.8 20.0 18.2 20.0 16.9
2.9 2.8 1.7 2.5 3.2 3.2 2.2
27.9 19.0 20.1 17.5 18.6 23.9 25.3
4.0 3.2 2.3 1.8 2.6 3.4 3.1
7.41 42.3 41.7 21.4 33.3 45.2 57.1
100 53.8 100 15.0 66.7 6.5 7.0
3.7 19.2 16.7 7.7 26.7 19.4 21.4
0.11 1.27 0.83 1.00 1.27 1.08 1.00
0.0 34.6 0.0 61.5 40.0 3.2 0.0
G MF-G G MF-B MF-G G G
Extant bison Plains bison (Bison bison bison) (1) Wood bison (Bison bison athabascae) (2) European bison (Bison bonasus)
mP mW mE
18 8 11
3.5 21.3 21.3
1.3 3.9 3.9
24.8 19.8 19.7
5.7 2.8 3.5
38.9 0 72.7
94.0 0 18.2
5.6 0 45.5
1.06 0.50 1.09
5.6 12.5 18.2
G G G
Abbreviations: PIT ¼ average number of pits; SCR ¼ average number of scratches; SD ¼ standard deviation; %LP ¼ percentage of large pits; %CS ¼ percentage of cross-scratches; %G ¼ percentage of gouge; SWS ¼ scratch width score from 0 to 2 (0 ¼ fine scratches only to 2 ¼ coarse scratches only); %0e17 ¼ low-scratch percentage i.e. number of specimens with scratches count between 0 and 17; G ¼ grazer; MF-G ¼ Graze-dominated mixed feeder; MF-B ¼ browse-dominated mixed feeder. (1) Microwear data from Solounias and Semprebon (2002); (2) Microwear data from Rivals et al. (2007).
between 0 and 17) and grazers (0e22.2% of scratches fall between 0 and 17) studied. Importantly, no overlap is seen in the ranges of browsers and seasonal or regional mixed feeders and very little overlap is seen between grazers and seasonal or regional mixed feeders (20.93e70% of scratches fall between 0 and 17). It is clear from examining Figs. 2 and 3 that none of the extant or fossil bison studied have results consistent with a pure browsing diet as average scratch and pit values for bison fall outside of the typical extant browsing average scratch/pit morphospace boundaries. However, as mentioned above, average scratch and pit data do not effectively discriminate many mixed feeders that alternate their dietary habits regionally or seasonally. Thus raw scratch data such as low-scratch range values are more effective in sorting extant taxa into more discrete dietary categories. Fig. 3 shows that the modern plains and wood bison have raw scratch results typical of modern grazers as does fossil B. antiquus from Plainview Quarry and Dalhart Sideroad Pit (Texas) as well as from
Fig. 2. Bivariate diagram based on microwear signatures (average number of pits versus average number of scratches) in extant and fossil bison. Microwear obtained at 35 magnification with a stereomicroscope. Gray areas correspond to the Gaussian confidence ellipses (p ¼ 0.95) for extant leaf browsing taxa (B) and extant grazing taxa (G) (extant data from Solounias and Semprebon, 2002). Error bars represent standard deviation for the mean of pit and scratch numbers. Abbreviations for the bison samples see Table 2.
Fairbanks Area (Alaska) and Folsom Quarry (New Mexico). However, fossil B. antiquus from Ingleside (Texas) and from Blackwater Draw (New Mexico) and Seminole Field (Florida) have raw scratch results more typical of extant mixed feeders. 4. Discussion The extant bison analyzed (i.e., plains bison e B. b. bison, wood bison e Bison bison athabascae, and European bison e Bison bonasus) all had microwear signatures typical of grazers. These findings were surprising given what is currently known about their feeding ecology (Meagher, 1986; Larter and Gates, 1991; Pucek, 2004). In contrast, the fossil bison samples analyzed have microwear signatures much more diverse. Whereas some of the bison samples exhibited the microscopic dietary traits of pure grazers (e.g., those from Fairbanks, Folsom Quarry, Plainview Quarry, and Dalhart Sideroad Pit) and similar to the extant plains bison (Bison bison bison), the other three samples analyzed showed microwear signatures with fewer scratches than found in extant grazers, and with raw scratch distributions typical of extant mixed feeders. Among the mixed feeding fossil bison, those from Ingleside and Blackwater Draw apparently were graze-dominated mixed feeders, while those from Florida had lower scratch results more typical of browse-dominated mixed feeders (Fig. 3). Results were somewhat surprising that these fossil bison exhibited a greater diversity of dietary habits than their extant relatives. This diversity observed in the fossil bison samples reflects a plasticity in feeding behavior that was suggested in a previous study by Rivals et al. (2007) on a small number of samples. These studies confirm that this finding is significant as extant bison ecology is often used as a typical model for extrapolating fossil bison ecology (Guthrie, 1970, 1990; Cannon, 2001; Johnson et al., 2005). The results of this study reveal two important things: (1) that a more variable dietary strategy was employed in late Pleistocene bison than is employed today for some reasons (i.e. some fossil bison were exclusive grazers while some alternated between browse and grass seasonally or regionally) and (2) modern populations of bison are not necessarily a good model for inferring bison paleoecology. This study shows that there is a risk involved when applying the uniformitarianism principle for reconstructions of paleoecology and paleoenvironments. The intra-population variability of scratch/pit results is rather low in the fossil samples, as illustrated by the standard deviation of each sample (Fig. 2). Except for the Ingleside and Blackwater Draw samples, the inter-population differences among samples are significant and there is no overlap in the microwear signals. The
F. Rivals, G.M. Semprebon / Quaternary International 245 (2011) 279e284
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Fig. 3. Low-scratch percentages (%0e17) for extant ungulates (grazers, leaf browsers, and mixed feeders) in comparison to the three species of extant bison and the seven fossil bison samples. Abbreviations for the bison samples see Table 2.
low intra-population variability is probably related to the method employed and the nature of the selected samples. With the exception of the sample from Fairbanks, most of the samples are from archaeological sites where the accumulations are related to Paleo-Indian (Clovis or Folsom) settlements of limited duration. Moreover, it is important to keep in mind that microwear analysis gives information about the last diets of animals. A correlation between microwear variability and duration of depositional events has been evidenced in the archaeological record (Rivals et al., 2009). Low variability was shown to be most likely the result of short occupational (or depositional) events, such as those observed in archaeological localities at Seminole Field, Ingleside, or Folsom Quarry. On the contrary, higher variability may correspond to longer depositional events such as those observed in the sample from Fairbanks where the fossil assemblage resulted from natural depositional events and fossils were collected on very large areas (Stephenson et al., 2001). The microwear signal is consequently a proxy for the bison diet at the time the locality was occupied, and thus a good proxy for the local environmental conditions of the Paleo-Indians. 5. Conclusion Recently, many studies have demonstrated the potential and utility of microwear studies for paleoecological reconstructions. Microwear is a powerful tool because it offers high dietary resolution, is not affected by taxonomy, is non-destructive, and is sensitive to rapid changes in vegetation and climatic events. Improvements in the resolution of molding compounds have facilitated the sampling process in collections with restrictive sampling policies, and have allowed for the acquisition of large fossil tooth surface samples which has increased statistical power of recent studies. This study confirms that tooth microwear is a good proxy for characterizing the immediate behavior of ungulates, and thus the precise environmental conditions corresponding to the formation of the fossil assemblages, whether of natural or anthropic origin. It
is now obvious that extinct ungulate dietary traits are more diverse than previously expected from analysis of morphology (e.g. hypsodonty). This shows that data on the ecology of modern relatives does not necessarily precisely reflect the ecology of extinct species. The dietary plasticity observed is an important data to take into account in paleoenvironmental studies based on the ecological adaptations of ungulates. Acknowledgements We thank Hervé Bocherens for the invitation to submit this paper. We acknowledge the curators and collection managers at the institutions visited: J. Flynn, C. Norris, and J. Galkin (Division of Paleontology, AMNH, New York), E. Westwig (Division of Vertebrate Zoology, AMNH, New York), and T. Rowe and L.K. Murray (Vertebrate Paleontology Laboratory, University of Texas at Austin). FR was supported by a travel grant from the Spanish ministry of foreign affairs (Ministerio de Asuntos Exteriores y de Cooperación and AECID grant CF-262). This research received support from the SYNTHESIS Project http://www.synthesis.info/ which is financed by European Community Research Infrastructure Action under the FP7 Integrating Activities Programme (AT-TAF-4385 and GB-TAF59). GS was supported by Faculty Development Funds by Bay Path College. References Aguilar, J.-P., Legendre, S., Michaux, J., Montuire, S., 1999. Pliocene mammals and climatic reconstruction in the western Mediterranean area. In: Wrenn, J.H., Suc, J.-P., Leroy, S.A.G. (Eds.), The Pliocene: Time of Change. American Association of Stratigraphic Palynologists Foundation, Salt Lake City, pp. 109e120. Blois, J.L., Hadly, E.A., 2009. Mammalian response to Cenozoic climatic change. Annual Review of Earth and Planetary Sciences 37, 181e208. Cannon, K.P., 2001. What the past can provide: contribution of prehistoric bison studies to modern bison management. Great Plains Research 11, 145e174. DeGusta, D., Vrba, E., 2005. Methods for inferring paleohabitats from discrete traits of the bovid postcranial skeleton. Journal of Archaeological Science 32, 1115e1123. Feranec, R.S., 2007. Ecological generalization during adaptive radiation: evidence from Neogene mammals. Evolutionary Ecology Research 9, 555e577.
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Rensberger, J.M., 1978. Scanning electron microscopy of wear and occlusal events in some small herbivores. In: Butler, P.M., Joysey, K.A. (Eds.), Development, Function and Evolution of Teeth. Academic Press, London, pp. 415e438. Rivals, F., Schulz, E., Kaiser, T.M., 2008. Climate-related dietary diversity of the ungulate faunas from the middle Pleistocene succession (OIS 14-12) at the Caune de l’Arago (France). Paleobiology 34, 117e127. Rivals, F., Schulz, E., Kaiser, T.M., 2009. A new application of dental wear analyses: estimation of duration of hominid occupations in archaeological localities. Journal of Human Evolution 56, 329e339. Rivals, F., Solounias, N., 2007. Differences in tooth microwear of populations of caribou (Rangifer tarandus, Ruminantia, Mammalia) and implications to ecology, migration, glaciations and dental evolution. Journal of Mammalian Evolution 14, 182e192. Rivals, F., Solounias, N., Mihlbachler, M.C., 2007. Evidence for geographic variation in the diets of late Pleistocene and early Holocene Bison in North America, and differences from the diets of recent Bison. Quaternary Research 68, 338e346. Sellards, E.H., Evans, G.L., Meade, G.E., 1947. Fossil bison and associated artifacts from Plainview, Texas. Geological Society of America Bulletin 58, 927e954. Semprebon, G., Janis, C., Solounias, N., 2004a. The diets of the Dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change. Journal of Vertebrate Paleontology 24, 427e444. Semprebon, G.M., Godfrey, L.R., Solounias, N., Sutherland, M.R., Jungers, W.L., 2004b. Can low-magnification stereomicroscopy reveal diet? Journal of Human Evolution 47, 115e144. Semprebon, G.M., Rivals, F., 2007. Was grass more prevalent in the pronghorn past? An assessment of the dietary adaptations of Miocene to recent Antilocapridae (Mammalia: Artiodactyla). Palaeogeography, Palaeoclimatology, Palaeoecology 253, 332e347. Semprebon, G.M., Rivals, F., 2010. Trends in the paleodietary habits of fossil camels from the tertiary and quaternary of North America. Palaeogeography, Palaeoclimatology, Palaeoecology 295, 131e145. Solounias, N., Semprebon, G., 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. American Museum Novitates 3366, 1e49. Stephenson, R.O., Gerlach, S.G., Guthrie, R.D., Harington, C.R., Mills, R.O., Hare, G., 2001. Wood bison in late Holocene Alaska and adjacent Canada: paleontological, archaeological and historical records. In: Gerlach, S.G., Murray, M.S. (Eds.), People and Wildlife in Northern North America: Essays in Honor of R. Dale Guthrie. Archaeo Press, Oxford, pp. 125e159. Vrba, E.S., 1988. The significance of bovid remains as indicators of environment and predation patterns. In: Behrensmeyer, A.K., Hill, A.P. (Eds.), Fossils in the Making: Vertebrate Taphonomy and Paleoecology. The University of Chicago Press, Chicago, pp. 247e271. Walker, A., Hoek, H.N., Perez, L., 1978. Microwear of mammalian teeth as an indicator of diet. Science 201, 908e910. Webb, S.D., 1974. Pleistocene Mammals of Florida. The University Presses of Florida, Gainesville. Wilkerson, A.S., 1932. Some frozen deposits in the goldfields of interior Alaska. A study of the Pleistocene deposits of Alaska. American Museum Novitates 525, 1e22.
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Quaternary International journal homepage: www.elsevier.com/locate/quaint
Dietary plasticity in ungulates: Insight from tooth microwear analysis Florent Rivals a, b, c, *, Gina M. Semprebon d a
ICREA, Barcelona, Spain IPHES, Institut Català de Paleoecologia Humana i Evolució Social, C/ Escorxador s/n, 43003 Tarragona, Spain c Area de Prehistoria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain d Bay Path College, 588 Longmeadow Street, Longmeadow, MA 01106, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 7 August 2010
In recent years, tooth microwear has been used as a powerful tool for investigating mammalian diets in paleontological or archaeological contexts. Tooth microwear techniques were applied to a number of late Pleistocene assemblages of bison (Bison antiquus) from North America to analyze bison dietary traits, but more particularly, to test for dietary plasticity of the fossil species compared to their modern relatives. Modern bison species are known to be grazers from their ecology. However, the results from tooth wear analysis indicate that dietary traits were more diverse in the fossil bison than in their modern relatives. Bison paleodiets range from pure grazing to mixed feeding. The results illustrate not only the dietary plasticity for that species, but also the potential implications involved when using modern species as analogues for reconstructing the ecology of fossil species. Tooth microwear is a good proxy in archaeological contexts because it gives an insight on the diet of the last days of an animal’s life. The intra-population variability in diet is discussed in relation to the duration of formation of the assemblages (natural assemblages versus archaeological Paleo-Indian sites). Ó 2010 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Mammal ecology is frequently investigated through a number of proxies (e.g. locomotion, diet). Insights gained via such proxies are frequently used in paleoenvironmental reconstructions and also for tracking climatic shifts through time (Janis, 1984, 1993, 2003; Vrba, 1988; Aguilar et al., 1999; DeGusta and Vrba, 2005). Morphologic change is one of the most commonly documented responses to ecological changes in the continental fossil record of mammals. Bones and teeth of mammals conveniently preserve important information about two traits e locomotion and diet e both of which play an important role in deciphering the evolutionary history of mammals (Janis, 1984, 2003, 2008). Climatic impact on the evolution of mammals is actually a highly complex phenomenon. It seems reasonable to suppose that both climate change and intrinsic biotic controls would have contributed to faunal evolution, although at different temporal scales and magnitudes. Thus, the response of large mammals to climatic changes is usually synchronous but it may also be asynchronous at times. In the latter case, a discrepancy or time lag may exist between climatic events and changes in mammals. Such * Corresponding author. IPHES, Institut Català de Paleoecologia Humana i Evolució Social, C/ Escorxador s/n, 43003 Tarragona, Spain. Fax: þ34 977 55 95 97. E-mail address: fl[email protected] (F. Rivals). 1040-6182/$ e see front matter Ó 2010 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2010.08.001
a discrepancy may not only result from issues involving differences in time scale and temporal resolution but also may be due to the specific proxy used. For example, changes in skull morphology and tooth wear in the extinct artiodactyl group known as the Dromomerycidae suggested an adjustment in diet during the late Miocene to Pliocene increase in aridity in North America; however, skull morphology apparently lagged behind the apparent dietary shift which was revealed through microwear and mesowear analyses (Semprebon et al., 2004a). Isotope studies reveal that dietary changes may also be more labile than morphologic changes (Feranec, 2007), an insight that may explain the lack of temporal synchronicity between changes in tooth shape and wear (Rivals et al., 2007, 2008; Semprebon and Rivals, 2007, in press; Janis, 2008; Joomun et al., 2008). Similar lags or decoupling between climatic change and various aspects of morphology is very frequently observed in the Pleistocene and Holocene (Kaiser and Franz-Odendaal, 2004; Kaiser and Schulz, 2004; Rivals and Solounias, 2007; Semprebon and Rivals, 2010). It seems evident that speciation events and morphological changes are not necessarily the best ecological proxies, especially when applied to the Quaternary, because morphology (thus speciation) requires many generations for a character to be fixed in a population. In the same way, not all species will exhibit changes in their geographic ranges during periods of climatic change (Blois and Hadly, 2009). Therefore, the biotic response of individuals, species,
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and communities to climatic change is a highly complex phenomenon. Thus, an understanding of more immediate traits, and in particular environments, is an important future research direction and specific procedures such as stable isotopes or dental microwear analyses should be employed to fully understand this phenomenon. Importantly, both tooth microwear and stable isotope analyses are not related to phylogeny, and, therefore, they both reflect the immediate behavior of an animal. In contrast to gross morphology, microscopic tooth wear gives insight into the dietary behavior of the last days or weeks before death, and consequently it provides a snapshot of the environmental condition present at the time the animals were living. Moreover, tooth wear techniques are often preferred over stable isotopes because they are neither destructive nor invasive. This is an important advantage because there are strong destructive sampling policies restricting such work in many collections today. To cope with the decoupling frequently observed between climatic change and various aspects of morphology, tooth microwear analysis is a suitable mechanism for investigating ungulate diets. The diet of extinct ungulates provides valuable information about the food resources available in a given habitat and thus reconstructing paleodiet provides a useful tool for reconstructing paleohabitats. Additionally, information about the diet of extinct ungulates provides insight into resource partitioning and dietary behavior of entire ungulate populations and communities. Consequently, the data can be used to make inferences on differential dietary regimes and seasonal fluctuation in diets. The objective of this paper is to analyze bison dietary traits in the North American late Pleistocene fossil record, and more particularly to evaluate the dietary plasticity of the extinct species in comparison to their modern relatives. A previous study by Rivals et al. (2007) reported geographical differences in diets in four samples of extinct bison. To expand upon that analysis, seven samples of bison (Bison antiquus) from the late Pleistocene of North America were studied (Table 1). The samples come from four States and are identified using the State code followed by a number if several exist for a state: Alaska (AK), Florida (FL), New Mexico (NM1 and NM2), and Texas (TX1, TX2, and TX3). 2. Methodology: tooth wear, a non-destructive proxy for reconstructing diet in fossil ungulates In this study, microscopic analysis of dental wear patterns is used to provide a direct source of evidence for the nature of tooth
use in fossil bison. The microscopic defects on occlusal enamel (microwear) are analyzed here and represent a true snapshot of dietary behavior, sometimes representing the animals’ last meals consumed (last days or week). The high degree of functional similarity in occlusal mechanics for unimodal chewing systems of many herbivorous ungulates provides the prerequisite for an interpretation of microwear patterns as a trophic signal. 2.1. Molding technique Data collection is undertaken using molding and casting techniques. The methodology is adapted from long-standing dental procedural technology. In order to gain high resolution casts, molds are made using fast setting silicone molding materials with low shrinkage. Due to their excellent resolution, such molds can be used for microwear investigation. Making tooth impressions as described does not harm recent or fossil dental tissues because the silicone impression materials used are chemically inert. The method is thus non-destructive. 2.2. Tooth microwear analysis Microwear analysis involves observing the microscopic scars on enamel (Fig. 1) produced by food (phytoliths present in the leaves, grasses, or fruit and seed coats) and grit or dust present on the surface of vegetation. Tooth microwear research originated in the late 1970s using scanning electron microscopes (Rensberger, 1978; Walker et al., 1978) and was later applied to a large variety of taxa. Solounias and Semprebon (2002) proposed a new and greatly simplified methodology for the assessment of the dietary adaptations of living and fossil taxa. This method was developed to allow for microwear scar topography to be accurately analyzed at low magnification (35) using a standard stereomicroscope (Semprebon et al., 2004b). They presented a comparative microwear database of extant artiodactyls, perissodactyls, and proboscideans and interpreted the data to elucidate the diets of these extant ungulates. This database, extended by Semprebon and Rivals, now consists of 76 modern ungulate species. Microwear analysis following the light microscopic protocol by Solounias and Semprebon (2002) was undertaken using a stereomicroscope Zeiss Stemi 2000-C, which has been established as one of the standard forms of equipment for this approach. Microwear is examined on the second enamel band of the paracone of the upper M2 or the protoconid of the lower m2 of adult
Table 1 Description and age of the samples analyzed. Sample locality
Museum curation
Age
Fairbanks area, Alaskaa
Frick Collection at the American Museum of Natural History, New York Frick Collection at the American Museum of Natural History, New York Texas Memorial Museum, Austin, Texas (TMM locality 42345)
Radiocarbon dated to 11,990 135 14C yr B.P. (Stephenson et al., 2001) Rancholabrean North American Land Mammal Age (Webb, 1974) Rancholabrean (late Pleistocene) North American Land Mammal Age (Hester, 1972)
Frick Collection at the American Museum of Natural History, New York
Radiocarbon dated on bone amino acids from different individuals in the bison sample indicating an average age of approximately 10,500 14C yr B.P. (Meltzer et al., 2002) Rancholabrean (late Pleistocene) North American Land Mammal Age (Lundelius, 1972; Otvos and Howat, 1996). Excavated in the 1940’s and yielded the Plainview cultural material which is 10,000 B.P., but most likely late or postFolsom (Holliday, 1985; Holliday et al., 1999; Sellards et al., 1947) Labeled as late Pleistocene in the archives at the AMNH but no other data is available
Seminole field station B, Pinellas County, Florida Blackwater draw locality no. 1, Clovis gravel pit, Curry C., New Mexicob Folsom Quarry, Union County, New Mexico Ingleside fauna, San Patricio County, Texas (TMM locality 30967) Plainview Quarry, Hale County, Texas
Dalhart Sideroad Pit, Hartley County, Texas a b
Texas Memorial Museum, Austin, Texas Texas Memorial Museum, Austin, Texas (TMM locality 725)
Frick Collection at the American Museum of Natural History, New York
Recovered from frozen deposits (Wilkerson, 1932). Contains a stratigraphic sequence with Clovis, Folsom, and other artifacts as well as Rancholabrean faunal remains (Hester, 1972).
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281
Fig. 1. Occlusal enamel surface of extant (A) and fossil (B) bison teeth at 35. (A) Modern wood bison, Bison bison athabascae (AMNH 86950). (B) Fossil bison, Bison priscus from Folsom Quarry, New Mexico (AMNH 131563).
individuals (young and old adults were discarded). Transparent epoxy casts are examined at 35 magnification using a stereomicroscope using oblique lighting from above the cast. Under the light microscope, pits and scratches are identified and counted within a standard area of 0.16 mm2 on the enamel band following the criteria of Semprebon et al. (2004b). Pits are microwear scars that are circular or sub-circular in outline and thus have approximately similar widths and lengths. Scratches are elongated microfeatures. They are not merely longer than they are wide, but they have straight, parallel sides. Two representative locations are counted because microwear is somewhat variable on a single tooth. The selected second band used here is intermediate in terms of the amount of wear features observed. The number of pits versus scratches for each individual per taxon is recorded. Typical grazers have the highest numbers of scratches and the lowest numbers of pits; typical leaf browsers have lower numbers of scratches and more disparate numbers of pits. Other microwear features are scored with the intent of providing a mechanism to further refine the dietary categorization of ungulates beyond the broad categories of browser versus grazer versus mixed feeder (Solounias and Semprebon, 2002). Table 2 summarizes the microwear variables scored and the type of information that can be gleaned from them.
3. Results A total of 169 teeth of B. antiquus were analyzed. Microwear results are summarized in Table 3. Fig. 2 represents dietary patterns of microwear seen in extant grazers, browsers, and mixed feeders (after Solounias and Semprebon, 2002) and in the extant and fossil bison studied here. The average number of scratches versus the average number of pits per taxon is shown (at 35 magnification). Gray areas delineate extant browsing and grazing scratch/pit morphospaces. It is clear in Fig. 2 that there is no overlap in microwear results between the extant grazing and browsing taxa. Some ungulates, however, are mixed feeders, that is, they switch from browse to grass seasonally or regionally. Consequently, they often fall in the gap between grazers and browsers in terms of average number of scratches but they may have average scratch values that overlap with those of browsers or grazers depending on whether they typically consume relatively more browse or grass.
Because seasonal and regional mixed feeders may have average scratch and pit results that overlap those of browsers and grazers additional calculations are necessary to discriminate them from other trophic groups. While such mixed feeding taxa typically display bimodal scratch distributions when individual raw scratch results are graphed (Solounias and Semprebon, 2002), a simple calculation accords good separation between extant browsers, grazers, and mixed feeders. The percentage of individuals per taxon possessing scratch numbers between 0 and 17 (i.e., the percentage of scratches per taxon that fall in the low-scratch range) offers good dietary resolution of the three main ungulate trophic groups (Semprebon and Rivals, 2007). These low raw scratch percentage results are summarized in Fig. 3 which shows the low-scratch percentage range of scores of extant browsers, grazers, and seasonal/regional mixed feeders as well as the extant and fossil bison studied here. The only overlap that occurs between trophic groups occurs between grazers and seasonal/regional mixed feeders. There is no overlap between the low-scratch ranges of the extant leaf-dominated browsers (72.73e100% of scratches fall
Table 2 Description of typical microwear results for extant ungulates on known diet. Microwear variable
Leaf browsers
Grazers
Mixed feeders
Fruit browsers
Average scratch count Average pit count Large pitsd Raw scratch distribution Puncture pitsd Scratch textured
Low
High
Variable
Variable
Lowa
Low
Variable
High
Low Unimodal elow Absent Fineb
Moderate Unimodal ehigh Absent Coarse or mixed Variablec
Moderate Bimodal (high and low) Absent Coarse or mixedb Variablec
High Variable
Gougingd
Variablec
Present Coarse, mixedb Variablec
Note: scratches that run in a horizontal or oblique direction in relation to the enamel band e i.e., cross-scratches provide information relevant to jaw mechanics and are also noted. a Except in dirty browsing (e.g., camels). b May see hypercoarse scratches in bark consumers (e.g., black rhinoceros) or hard fruit and seed consumers. c Generally higher in taxa encountering grit in foods (e.g., camels, pronghorn, vicuña). d From Solounias and Semprebon (2002).
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Table 3 Microwear summary data for the M2 of fossil and extant bison samples. Sample
Code
N
PIT
SD
SCR
SD
%LP
%CS
%G
SWS
%0e17
Diet
Fossil bison Fairbanks Area, Alaska Blackwater Draw, Clovis Pit, NM Folsom Quarry, New Mexico Seminole Field Station B, Florida Ingleside, Texas Plainview Quarry, Texas Dalhart Sideroad Pit, Texas
AK NM1 NM2 FL TX1 TX2 TX3
27 26 12 13 15 62 14
11.4 17.3 10.8 20.0 18.2 20.0 16.9
2.9 2.8 1.7 2.5 3.2 3.2 2.2
27.9 19.0 20.1 17.5 18.6 23.9 25.3
4.0 3.2 2.3 1.8 2.6 3.4 3.1
7.41 42.3 41.7 21.4 33.3 45.2 57.1
100 53.8 100 15.0 66.7 6.5 7.0
3.7 19.2 16.7 7.7 26.7 19.4 21.4
0.11 1.27 0.83 1.00 1.27 1.08 1.00
0.0 34.6 0.0 61.5 40.0 3.2 0.0
G MF-G G MF-B MF-G G G
Extant bison Plains bison (Bison bison bison) (1) Wood bison (Bison bison athabascae) (2) European bison (Bison bonasus)
mP mW mE
18 8 11
3.5 21.3 21.3
1.3 3.9 3.9
24.8 19.8 19.7
5.7 2.8 3.5
38.9 0 72.7
94.0 0 18.2
5.6 0 45.5
1.06 0.50 1.09
5.6 12.5 18.2
G G G
Abbreviations: PIT ¼ average number of pits; SCR ¼ average number of scratches; SD ¼ standard deviation; %LP ¼ percentage of large pits; %CS ¼ percentage of cross-scratches; %G ¼ percentage of gouge; SWS ¼ scratch width score from 0 to 2 (0 ¼ fine scratches only to 2 ¼ coarse scratches only); %0e17 ¼ low-scratch percentage i.e. number of specimens with scratches count between 0 and 17; G ¼ grazer; MF-G ¼ Graze-dominated mixed feeder; MF-B ¼ browse-dominated mixed feeder. (1) Microwear data from Solounias and Semprebon (2002); (2) Microwear data from Rivals et al. (2007).
between 0 and 17) and grazers (0e22.2% of scratches fall between 0 and 17) studied. Importantly, no overlap is seen in the ranges of browsers and seasonal or regional mixed feeders and very little overlap is seen between grazers and seasonal or regional mixed feeders (20.93e70% of scratches fall between 0 and 17). It is clear from examining Figs. 2 and 3 that none of the extant or fossil bison studied have results consistent with a pure browsing diet as average scratch and pit values for bison fall outside of the typical extant browsing average scratch/pit morphospace boundaries. However, as mentioned above, average scratch and pit data do not effectively discriminate many mixed feeders that alternate their dietary habits regionally or seasonally. Thus raw scratch data such as low-scratch range values are more effective in sorting extant taxa into more discrete dietary categories. Fig. 3 shows that the modern plains and wood bison have raw scratch results typical of modern grazers as does fossil B. antiquus from Plainview Quarry and Dalhart Sideroad Pit (Texas) as well as from
Fig. 2. Bivariate diagram based on microwear signatures (average number of pits versus average number of scratches) in extant and fossil bison. Microwear obtained at 35 magnification with a stereomicroscope. Gray areas correspond to the Gaussian confidence ellipses (p ¼ 0.95) for extant leaf browsing taxa (B) and extant grazing taxa (G) (extant data from Solounias and Semprebon, 2002). Error bars represent standard deviation for the mean of pit and scratch numbers. Abbreviations for the bison samples see Table 2.
Fairbanks Area (Alaska) and Folsom Quarry (New Mexico). However, fossil B. antiquus from Ingleside (Texas) and from Blackwater Draw (New Mexico) and Seminole Field (Florida) have raw scratch results more typical of extant mixed feeders. 4. Discussion The extant bison analyzed (i.e., plains bison e B. b. bison, wood bison e Bison bison athabascae, and European bison e Bison bonasus) all had microwear signatures typical of grazers. These findings were surprising given what is currently known about their feeding ecology (Meagher, 1986; Larter and Gates, 1991; Pucek, 2004). In contrast, the fossil bison samples analyzed have microwear signatures much more diverse. Whereas some of the bison samples exhibited the microscopic dietary traits of pure grazers (e.g., those from Fairbanks, Folsom Quarry, Plainview Quarry, and Dalhart Sideroad Pit) and similar to the extant plains bison (Bison bison bison), the other three samples analyzed showed microwear signatures with fewer scratches than found in extant grazers, and with raw scratch distributions typical of extant mixed feeders. Among the mixed feeding fossil bison, those from Ingleside and Blackwater Draw apparently were graze-dominated mixed feeders, while those from Florida had lower scratch results more typical of browse-dominated mixed feeders (Fig. 3). Results were somewhat surprising that these fossil bison exhibited a greater diversity of dietary habits than their extant relatives. This diversity observed in the fossil bison samples reflects a plasticity in feeding behavior that was suggested in a previous study by Rivals et al. (2007) on a small number of samples. These studies confirm that this finding is significant as extant bison ecology is often used as a typical model for extrapolating fossil bison ecology (Guthrie, 1970, 1990; Cannon, 2001; Johnson et al., 2005). The results of this study reveal two important things: (1) that a more variable dietary strategy was employed in late Pleistocene bison than is employed today for some reasons (i.e. some fossil bison were exclusive grazers while some alternated between browse and grass seasonally or regionally) and (2) modern populations of bison are not necessarily a good model for inferring bison paleoecology. This study shows that there is a risk involved when applying the uniformitarianism principle for reconstructions of paleoecology and paleoenvironments. The intra-population variability of scratch/pit results is rather low in the fossil samples, as illustrated by the standard deviation of each sample (Fig. 2). Except for the Ingleside and Blackwater Draw samples, the inter-population differences among samples are significant and there is no overlap in the microwear signals. The
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Fig. 3. Low-scratch percentages (%0e17) for extant ungulates (grazers, leaf browsers, and mixed feeders) in comparison to the three species of extant bison and the seven fossil bison samples. Abbreviations for the bison samples see Table 2.
low intra-population variability is probably related to the method employed and the nature of the selected samples. With the exception of the sample from Fairbanks, most of the samples are from archaeological sites where the accumulations are related to Paleo-Indian (Clovis or Folsom) settlements of limited duration. Moreover, it is important to keep in mind that microwear analysis gives information about the last diets of animals. A correlation between microwear variability and duration of depositional events has been evidenced in the archaeological record (Rivals et al., 2009). Low variability was shown to be most likely the result of short occupational (or depositional) events, such as those observed in archaeological localities at Seminole Field, Ingleside, or Folsom Quarry. On the contrary, higher variability may correspond to longer depositional events such as those observed in the sample from Fairbanks where the fossil assemblage resulted from natural depositional events and fossils were collected on very large areas (Stephenson et al., 2001). The microwear signal is consequently a proxy for the bison diet at the time the locality was occupied, and thus a good proxy for the local environmental conditions of the Paleo-Indians. 5. Conclusion Recently, many studies have demonstrated the potential and utility of microwear studies for paleoecological reconstructions. Microwear is a powerful tool because it offers high dietary resolution, is not affected by taxonomy, is non-destructive, and is sensitive to rapid changes in vegetation and climatic events. Improvements in the resolution of molding compounds have facilitated the sampling process in collections with restrictive sampling policies, and have allowed for the acquisition of large fossil tooth surface samples which has increased statistical power of recent studies. This study confirms that tooth microwear is a good proxy for characterizing the immediate behavior of ungulates, and thus the precise environmental conditions corresponding to the formation of the fossil assemblages, whether of natural or anthropic origin. It
is now obvious that extinct ungulate dietary traits are more diverse than previously expected from analysis of morphology (e.g. hypsodonty). This shows that data on the ecology of modern relatives does not necessarily precisely reflect the ecology of extinct species. The dietary plasticity observed is an important data to take into account in paleoenvironmental studies based on the ecological adaptations of ungulates. Acknowledgements We thank Hervé Bocherens for the invitation to submit this paper. We acknowledge the curators and collection managers at the institutions visited: J. Flynn, C. Norris, and J. Galkin (Division of Paleontology, AMNH, New York), E. Westwig (Division of Vertebrate Zoology, AMNH, New York), and T. Rowe and L.K. Murray (Vertebrate Paleontology Laboratory, University of Texas at Austin). FR was supported by a travel grant from the Spanish ministry of foreign affairs (Ministerio de Asuntos Exteriores y de Cooperación and AECID grant CF-262). This research received support from the SYNTHESIS Project http://www.synthesis.info/ which is financed by European Community Research Infrastructure Action under the FP7 Integrating Activities Programme (AT-TAF-4385 and GB-TAF59). GS was supported by Faculty Development Funds by Bay Path College. References Aguilar, J.-P., Legendre, S., Michaux, J., Montuire, S., 1999. Pliocene mammals and climatic reconstruction in the western Mediterranean area. In: Wrenn, J.H., Suc, J.-P., Leroy, S.A.G. (Eds.), The Pliocene: Time of Change. American Association of Stratigraphic Palynologists Foundation, Salt Lake City, pp. 109e120. Blois, J.L., Hadly, E.A., 2009. Mammalian response to Cenozoic climatic change. Annual Review of Earth and Planetary Sciences 37, 181e208. Cannon, K.P., 2001. What the past can provide: contribution of prehistoric bison studies to modern bison management. Great Plains Research 11, 145e174. DeGusta, D., Vrba, E., 2005. Methods for inferring paleohabitats from discrete traits of the bovid postcranial skeleton. Journal of Archaeological Science 32, 1115e1123. Feranec, R.S., 2007. Ecological generalization during adaptive radiation: evidence from Neogene mammals. Evolutionary Ecology Research 9, 555e577.
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