Dietary ecospace and the diversity of euprimates during the Early and Middle Eocene.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 126:237–249 (2005) Dietary Ecospace and the Diversity of Euprimates During the Early and Middle Eocene Christopher C. Gilbert* Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, New York 11794 KEY WORDS adapoid; omomyoid; ecomorphology; biogeography; diet; body size ABSTRACT This study examined adapoid and omomyoid euprimate dietary and body size diversity from the Eocene of North America and Europe. Estimates of body weights and shearing quotients calculated from lower molars were plotted on a coordinate graph as a representation of dietary niche space (dietary ecospace) occupied by extinct species. By computing the areas, average intertaxon distances, and average distances from the centroid of the resulting polygons, comparisons of Eocene euprimate dietary and body size diversity were made. Results indicate that euprimate dietary niche space expanded significantly in North America from the Early to Middle Eocene, and at all times during the Early and Middle Eocene, the niche space occupied by North American euprimates exceeded that of corresponding European euprimates. These results conﬁrm that fossil euprimate diversity, as mea- During the Eocene epoch (⬇55–35 Ma), euprimates were found as abundant members of both the North American and European faunas. Two distinct phylogenetic groups of euprimates were present in both biogeographic areas during this time: the lemur-like adapoids and the more tarsier-like omomyoids. While there have been numerous studies on the paleoecology of both biogeographic regions (e.g., Gunnell, 1997), the phylogeny and systematics of the primate species found there (e.g., Beard, 1988; Bown and Rose, 1987, 1991; Legendre et al., 1991; Williams and Covert, 1994; Godinot, 1998; Zonneveld et al., 2000), and the transition of species at the Early and Middle Eocene boundaries (e.g., Maas et al., 1995; Gunnell, 1995, 1997), none of these attempted to reconstruct and compare the total ecological diversity among preserved taxa on either of these continents. Previously, euprimate diversity during the Eocene epoch was examined only in terms of body size diversity and taxonomic diversity. Fleagle (1978) examined body size distributions among the two major superfamilies of euprimates that existed during this time, the Adapoidea and Omomyoidea. Covert (1986) extended the sample of Fleagle (1978) to include 73 Eocene taxa, and while some overlap existed between the groups, the result remained the © 2004 WILEY-LISS, INC. sured by diet and body size, signiﬁcantly differed across biogeographic areas. There are many possible explanations as to why North American euprimates were signiﬁcantly more diverse in terms of diet and body size than their European counterparts. The explanation advocated here as most responsible for the increased diversity during the Early and Middle Eocene relates to the existence and increased sampling of more ecologically diverse environments, such as basin margins in the western interior of North America. These diverse environments could have promoted biological processes that led to the generation of increased diversity in North America compared to the isolated island refugia of Western Europe during this time. Am J Phys Anthropol 126:237–249, 2005. © 2004 Wiley-Liss, Inc. same: adapoids and omomyoids were distinctly different in body size, and adapoids were, for the most part, larger than their omomyoid relatives. Gingerich (1981) and Fleagle (1999) also made an effort to plot body size through time, and compare the distribution of Eocene euprimates in Europe and North America. Fleagle (1999) noted both that the adapoid radiation started out at a larger body size than the omoyoid radiation and that the adapoids seemed to occupy adaptive niches more typical of modern primates, including large size, diurnality, frugivory, and folivory. It was also demonstrated that during the Eocene, the omomyoids of North America were more taxonomically diverse than the North American adapoids or the omomyoids of Europe (Gingerich, 1981; Fleagle, 1999). By constrast, in Europe, the exact opposite pattern was found: *Correspondence to: Christopher C. Gilbert, Department of Anthropology, SBS Building S-501, Stony Brook University, Stony Brook, NY 11794-4364. E-mail: email@example.com Received 29 May 2003; accepted 12 January 2004. DOI 10.1002/ajpa.20036 Published online 31 August 2004 in Wiley InterScience (www. interscience.wiley.com). 238 C.C. GILBERT European adapoids were more taxonomically diverse than European omomyoids or their North American adapoid relatives (Gingerich, 1981; Fleagle, 1999). Rather than simply looking at body size or taxonomic diversity, Fleagle and Reed (1996) analyzed extant primate total ecological diversity in terms of “ecospace” within and between the four major biogeographic areas inhabited by extant primates. The ecological niche that a species occupies is best imagined as a position in multivariate space deﬁned by an array of ecological variables such as diet, activity pattern, body size, and locomotor pattern (Hutchinson, 1978; Fleagle and Reed, 1996). Ecospace can then be visualized as a graphical representation of the range of ecological niches occupied by a group of species in the form of a polygon on an ecological multivariate plot. It can be thought to represent the collection or sum of the diversity of ecological niches occupied by a group of species in multivariate ecological space: a niche or kind of “superniche” at a higher biological level. While work has been undertaken concerning the study of extant primate communities and their ecological diversity (e.g., Charles-Dominique, 1975; Bouliere, 1985; Terborgh and van Schaik, 1987; Terborgh, 1992; Reed and Fleagle, 1995; Kappeler and Heymann, 1996), little has been done in the way of an analysis of fossil primate ecological diversity. The limitations of the fossil record in the preservation of many ecological niche variables (not to mention actual communities that existed in time and space) serve as a major deterrent to such an enterprise. Nonetheless, progress has been made. Godfrey et al. (1997) analyzed the ecospace of the extinct subfossil lemurs of Madagascar, and Gunnell (personal communication) as well as Gunnell and Ciochon (2003) have been attempting to reconstruct fossil primate “ecomorphospace” in Africa and Asia. The current study attempted to reconstruct and compare fossil euprimate ecological diversity from a portion of the Eocene, ⬇53– 48 Ma, spanning the period from the end of the Early Eocene to the beginning of the Middle Eocene of North America and Europe. This analysis differs from the aforementioned studies on Eocene euprimate body size diversity or taxonomic diversity because it attempts to include the ecological variable of diet in addition to body size, and because it attempts to restrict the comparison to the total preserved diversity of euprimates in North America and Europe during a more constrained and corresponding time period (rather than an entire epoch). Lower molar areas were taken as correlates of body size, and shearing quotients were used as indicators of dietary emphasis. The Early and Middle Eocene were chosen because they contained adequate information from similarsized geographic areas on both continents, thereby hopefully allowing for some control of geography and total geographical area sampled through time. As the fossil record does not provide information on all taxa for the variables of diet, locomotion, body size, and activity pattern, this study was restricted to the ecological variables of diet and body size in an analysis of diversity (in the form of dietary ecospace) for each euprimate assemblage. Body size and diet, however, are critical to the total ecological niche occupied by a species, and they were taken here as a rough proxy for total ecological diversity. For example, dietary variance is suggested by Fleagle (1999) to be one of the greatest differences among living primates, having signiﬁcant effects on aspects of their lives and morphologies. Therefore, the importance of diet for a species’ life history and overall ecology should not be underestimated. Nonetheless, it should be pointed out that future fossil ﬁnds of postcrania could signiﬁcantly alter our understanding of Eocene euprimates’ ecological niches, so the extension of dietary and body size diversity as a measure of total ecological diversity must be done with caution. That being said, the following hypotheses were evaluated: 1) Eocene euprimate dietary and body size diversity in different biogeographic areas differed signiﬁcantly (Fleagle and Reed, 1996). 2) Eocene euprimate dietary and body size diversity within biogeographic areas increased through time as the time since taxonomic divergence increased (Fleagle and Reed, 1999). METHODS Data collection Two general fossil-bearing regions, one from North America and one from Europe, were used to estimate Eocene fossil euprimate dietary and body size diversity. An attempt was made to restrict the analysis to a speciﬁc locality in each biogeographic area in order to reduce error potentially introduced from sampling multiple localities across a large biogeographic region (i.e., a continent). However, as no locality spanned the time period of interest in either geographic location, adjustments were made to include the taxa of several sites from a localized region: Wyoming from North America and France from Europe. These two regions sampled a similarsized total geographic area and a corresponding period of geologic time during the Early to Middle Eocene. Localities sampled from Wyoming include the Bighorn Basin, Green River Basin, Washakie Basin, and South Pass, and they extensively documented Early and Middle Eocene faunas (e.g., Williams and Covert, 1994; Gunnell, 1995, 1997; Zonneveld et al., 2000; Muldoon and Gunnell, 2002). Localities sampled from France similarly documented Early and Middle Eocene faunas and include Quercy, Provence, and the Paris Basin (e.g., Russell et al., 1992; Godinot et al., 1992; Godinot, 1978, 1998). The main stratigraphic layers contain- EOCENE PRIMATE DIETARY DIVERSITY 239 Fig. 1. a: Oblique view of left lower second molar, illustrating six shearing crests measured in this study. b: Occlusal view of same tooth (from Strait, 1991). Fig. 2. Graphic representation of dietary and body size diversity among individual species within assemblages. a: Area of polygon. b: Average distance from centroid. c: Average intertaxon distance (from Fleagle and Reed, 1996). ing taxa analyzed in this study included the Wa-6 (⬇53 Ma), Wa-7 (⬇52–51 Ma), Br-1b (⬇50 Ma), and Br-2 (⬇48 Ma) layers from North America, and the MP 7 (⬇55 Ma) through MP12 (⬇45 Ma) layers from Europe (Lucas, 1998; Fleagle, 1999). Adapoid and omomyoid taxa included in the analysis are listed in the Appendix. To reconstruct Eocene euprimate dietary ecospace, estimates of body size and diet were analyzed. Since body size is signiﬁcantly correlated with M1 area (e.g., Gingerich et al., 1982; Conroy, 1987), body size was estimated from museum specimens by measuring M1 area (M1 length ⫻ M1 width) in square millimeters and taking the average M1 area for each taxon used in the analysis (Gingerich et al., 1982). Dietary emphasis was estimated through the calculation of shearing quotients (SQ) (Kay, 1975, 1984; Kay and Covert, 1984; Covert, 1985) for fossil specimens in combination with the aforementioned body size estimates. SQ’s were calculated by measuring the length of the six shearing crests on the lower second molar and summing them for an observed estimate of measured total shearing (MTS) (Fig. 1). Expected total shearing (ETS) was calculated from measuring lower M2 length and then using the prosimian regression: ln ETS ⫽ ln共M 2 L兲*0.99 ⫹ 0.683 (1) where M2 L is the second molar length in millimeters (Kirk and Simons, 2001). The SQ was then determined by the equation: 关共MTS ⫺ ETS兲/ETS兴*100 . (2) A positive SQ value combined with a body size under the threshold of 500 g (Kay, 1975, 1984) was considered indicative of a primarily insectivorous diet, while a positive SQ value combined with a body size above 500 g was considered indicative of a primarily folivorous one. In contrast, a negative SQ combined with a body size under 500 g was considered indicative of a mostly frugivorous/gumnivorous diet, and a negative SQ combined with a body size above 500 g suggested that the species was probably frugivorous. Where well-preserved museum specimens were not 240 C.C. GILBERT TABLE 1. t-tests for Early Eocene polygons from North America and Europe1 Euprimates from Early Eocene of North America Area Average intertaxon distance Average distance from centroid Wa-6: 71,385.00 (1) Wa-7: 148,470.0 (1) Pooled: 148,938.0 (1) Wa-6: 244.52 (45) Wa-7: 283.16 (153) Pooled: 261.72 (276) Wa-6: 191.83 (10) Wa-7: 282.88 (18) Pooled: 266.53 (24) Average intertaxon distance Average distance from centroid 174.86 (28) Average intertaxon distance Average distance from centroid P P P 127.43 (8) P P Wa-6: 11,224.00 (1) Wa-7: 12,486.00 (1) Pooled: 17,246.00 (1) Wa-6: 98.89 (21) Wa-7: 93.68 (78) Pooled: 91.90 (136) Wa-6: 61.99 (7) Wa-7: 66.46 (13) Pooled: 65.06 (17) Omomyoids from Early Eocene of Europe 1,938 (1) 107.55 (3) 58.00 (3) Adapoids from Early Eocene of North America Area Signiﬁcance 29,882.00 (1) Omomyoids from Early Eocene of North America Area Euprimates from Early Eocene of Europe Wa-6: 4,885.00 (1) Wa-7: 43,929.00 (1) Pooled: 53,448.00 (1) Wa-6: 205.84 (3) Wa-7: 285.91 (10) Pooled: 263.30 (21) Wa-6: 124.46 (3) Wa-7: 176.04 (5) Pooled: 170.84 (7) Adapoids from Early Eocene of Europe 12,501.00 (1) 178.63 (10) 113.45 (5) X X X ⫽ 0.035 ⬍ 0.000 ⬍ 0.000 n.s. ⬍ 0.000 ⬍ 0.000 Signiﬁcance X X X n.s. n.s. n.s. n.s. n.s. n.s. Signiﬁcance X X X n.s. n.s. n.s. n.s. n.s. n.s. 1 Sample sizes (n) appear in parentheses. n.s., nonsigniﬁcant result. X, no statistical test could be performed. available to measure, published data were used (for raw tooth measurements, body size estimates, and shearing quotients, see the Appendix). In an attempt to increase sample sizes, published data from sites outside the two biogeographic areas of focus were included as long as the taxon in question was also documented in Wyoming or France. Measured museum specimens were housed in either the American Museum of Natural History or the Comparative Anatomy Museum at Stony Brook University. Measurements were taken using a reticulated microscope lens, where available, or a combination of microscope and digital calipers. Where specimens were unavailable for measurement and calculation of an SQ, a conservative estimate in the form of a generic average was used. Data analysis The data for each taxon were placed on a bivariate plot with M1 area on the x-axis and shearing quotient on the y-axis. Plots were constructed for each biogeographic area, time period (Early or Middle Eocene), and stratigraphic layer for which information was available. Raw tooth area, rather than estimated body size, was plotted on the x-axis to eliminate any potentially introduced error. For the reader’s convenience, however, body size estimates for each taxon are provided in the Appendix. Even though the y-variable (shearing quotient) also has a lower molar tooth length component, there was no signiﬁcant correlation between SQ and M1 area. The minimum convex polygon was drawn around the pooled fossil primate taxa from each region and time period sampled as a representation of Eocene euprimate dietary ecospace. The area of the polygon, the average intertaxon distance, and the average distance from the centroid were used as quantiﬁcations of the dietary ecospace occupied by a given euprimate assemblage, and were seen as measures of dietary and body size diversity (Fleagle and Reed, 1996; Godfrey et al., 1997; see Fig. 2). Areas and distances were calculated using the SigmaScan software package, and differences between groups were tested for signiﬁcance using two-tailed t-tests (see Tables 1 and 2 for t-test results). To further examine the relationship between euprimate dietary and body size diversity, ecological distance, and time, regressions were performed between time and intertaxon distance as well as time and the average distance from the centroid; using taxa from stratigraphic layers of known approximate age (Wa-6 ⫽ 241 EOCENE PRIMATE DIETARY DIVERSITY TABLE 2. t-tests for Middle Eocene polygons from North America and Europe1 Euprimates from Middle Eocene of North America Area Average intertaxon distance Average distance from centroid Br-1b: 66,018.00 (1) Br-2: 108,930.00 (1) Pooled: 109,553.00 (1) Br-1b: 302.53 (21) Br-2: 331.70 (78) Pooled: 321.02 (153) Br-1b: 230.44 (7) Euprimates from Middle Eocene of Europe 27,560.00 (1) 157.73 (36) 111.67 (9) Omomyoids from Middle Eocene of North America Average intertaxon distance Average distance from centroid Br-1b: 8,944.00 (1) Br-2: 28,309.00 (1) Pooled: 28,932.00 (1) Br-1b: 118.79 (10) Br-2: 136.77 (36) Pooled: 122.61 (66) Br-1b: 76.98 (5) Omomyoids from Middle Eocene of Europe 1,952.00 (1) 67.34 (3) 38.87 (3) Br-2: 94.56 (9) Pooled: 88.20 (12) Average intertaxon distance Average distance from centroid Signiﬁcance X X X n.s. P ⬍ 0.000 P ⬍ 0.000 n.s. n.s. P ⫽ 0.003 Adapoids from Middle Eocene of North America Area P P P P X X X ⫽ 0.005 ⬍ 0.000 ⬍ 0.000 ⫽ 0.001 P ⫽ 0.005 P ⫽ 0.002 Br-2: 256.65 (13) Pooled: 254.65 (18) Area Signiﬁcance Br-1b: X Br-2: 7,428.00 (1) Pooled: 8374.00 (1) Br-1b: 174.10 (1) Br-2: 301.76 (6) Pooled: 238.69 (15) Br-1b: 87.05 (2) Adapoids from Middle Eocene of Europe 15,958.00 (1) 130.74 (15) 84.56 (6) Br-2: 184.60 (4) Pooled: 152.33 (6) Signiﬁcance X X X n.s. P ⫽ 0.041 P ⫽ 0.011 n.s. n.s. n.s. 1 Sample sizes (n) appear in parentheses. n.s., nonsigniﬁcant result. X, no statistical test could be performed. 53 Ma, Wa-7 ⫽ 51.5 Ma, Br-1b ⫽ 50 Ma, and Br-2 ⫽ 48 Ma). RESULTS Hypothesis 1: among biogeographic areas Hypothesis 1, that the dietary niche space (i.e., dietary ecospace) occupied by euprimates from different biogeographic areas differed signiﬁcantly, was supported. The total dietary niche space occupied by euprimates in the Early and Middle Eocene of North America differed greatly from that occupied by European euprimates during both time periods by all three measures used: area of the polygon, the average intertaxon distance, and the average distance from the centroid of the polygons (Tables 1 and 2). As is evident in Figures 3 and 4, North American euprimates took up a greater amount of dietary ecospace and were signiﬁcantly more diverse than their European counterparts during the Early and Middle Eocene. The greatest difference between North American and European euprimate dietary and body size diversity is explained by the larger, frugivorous and folivorous adapoid primates of North America (⬎1,000 g). European adapoid primates during this time period, in contrast, were almost all under 1,000 g. The overall difference between North American and European adapoid polygons by way of the three measures of dietary and body size diversity used, however, is not signiﬁcant in the Early Eocene, and only becomes signiﬁcant in the Middle Eocene. In the Middle Eocene, while the North American adapoid polygon was actually smaller in area than the European adapoid polygon, the average intertaxon distance of North American adapoid primates was signiﬁcantly greater than the average intertaxon distance of European adapoid primates (Table 2). These seemingly contradictory results reﬂect the fact that there was an increase among North American adapoid primates along the SQ axis (to relatively uniform and folivorous SQ), while body size increased only marginally. The resulting polygon was then stretched horizontally, decreasing in area while increasing in average intertaxon distance. Omomyoid primates from the Early Eocene of North America had a larger guild of small frugivo- 242 C.C. GILBERT Fig. 3 a: Early Eocene euprimate dietary ecospace from North America. For Figures 3– 6, total euprimate (adapoid ⫹ omomyoid) assemblages are outlined in dashed lines, omomyoid assemblages in solid lines, and adapoid assemblages in dotted lines. Individual data points are also displayed (see Appendix for individual taxon values). Kay’s threshold (1975, 1984) ⫽ 9.0 mm2 ⫽ 500 g. b: Early Eocene euprimate dietary ecospace from Europe. rous/gumnivorous taxa that resulted in a greater polygon area than that of corresponding Early Eocene European omomyoid assemblages (Table 1). Likewise, Middle Eocene omomyoids in North America were more diverse and had a much greater polygon area, a signiﬁcantly greater average intertaxon distance, and a signiﬁcantly greater average distance from the centroid than their Middle Eocene European counterparts (Table 2). North American omomyoids during the Middle Eocene exhibited a shift to larger body sizes and, in the case of one taxon, Hemiacodon gracilis, also included a signiﬁcant portion of leaves in the diet. During the Early and Middle Eocene, European omomyoids remained small and insectivorous. Hypothesis 2: within biogeographic areas Hypothesis 2, that the dietary and body size diversity exhibited within biogeographic areas expanded through time, was weakly supported. While North American euprimate dietary and body size diversity expanded in some respects from the Early Fig. 4. a: Middle Eocene euprimate dietary ecospace from North America. b: Middle Eocene euprimate dietary ecospace from Europe. to Middle Eocene (Figs. 3a, 4a), European euprimate dietary and body size diversity did not expand and, in fact, appeared to have even possibly contracted in terms of total dietary ecospace occupied (Figs. 3b, 4b). The North American euprimate expansion was signiﬁcant in terms of intertaxon distance from the Early to Middle Eocene (t ⫽ ⫺2.611, p ⫽ 0.009). The difference in dietary niche space occupied by European euprimates during the Early to Middle Eocene did not differ signiﬁcantly by any measure employed. While some North American adapoids shifted to a more folivorous diet during the transition from the Early to Middle Eocene (see, also, Covert, 1986), the differences between North American adapoid polygons were not signiﬁcant. In addition to a shift to folivory for many adapoids, one Middle Eocene omomyoid taxon probably also included a substantial portion of leaves in its diet. This expansion in omomyoid dietary ecospace is reﬂected in a greater overall polygon area (Figs. 3a, 4a; Tables 1 and 2). The other two measures of diversity did not detect any signiﬁcant differences between the Early and Middle Eocene omomyoid polygons, although the difference between the Early and Middle Eocene average intertaxon distances is on the cusp of signiﬁcance (t ⫽ ⫺1.965, p ⫽ 0.051). In addition to an apparent EOCENE PRIMATE DIETARY DIVERSITY 243 Fig. 5. Early Eocene euprimate dietary ecospace from North America. Fig. 6. Middle Eocene euprimate dietary ecospace from North America. dietary shift, the North American polygons seemed to expand in body size for both adapoid and omomyoid primates (Figs. 3a, 4a). To examine the North American polygons in further detail, these primate assemblages were broken down by stratigraphic layer in the Early and Middle Eocene, from the Wa-6 layer (⬇53 Ma) to the Wa-7 layer (⬇52–51 Ma) in the Early Eocene through the Br-1b layer (⬇50 Ma) to the Br-2 layer (⬇48 Ma) in the Middle Eocene (Szalay and Delson, 1979; Lucas, 1998). As is evident in Figures 5 and 6, within both the Early and Middle Eocene, euprimate dietary and body size diversity was not markedly different, except in the case of overall area between the Wa-6 and Wa-7 layers during the Early Eocene (Fig. 5, Table 1). The only signiﬁcant difference detected was between total euprimate assemblages as they expanded in terms of the average distance from the centroid from the Wa-6 to Wa-7 layer (t ⫽ ⫺2.616, p ⫽ 0.015). In addition, as the graphs show, the shape of the Early Eocene polygons and especially the Middle Eocene polygons were remarkably similar. This indicates two things. First, pooled data from either pair of these stratigraphic layers for an overall picture of Early and Middle Eocene dietary ecospace probably did not introduce signiﬁcantly large error into the study, and therefore either polygon or their pooled sum is a valid characterization of both Early and Middle Eo- cene North American primate dietary ecological diversity. To further justify the time-averaging involved in pooling the data from adjacent stratigraphic layers, each individual assemblage from the four North American stratigraphic layers was individually compared against its corresponding pooled European assemblage. Every North American euprimate polygon was still signiﬁcantly greater in terms of intertaxon distance, and all but one was also still signiﬁcantly greater in terms of distance from the centroid (Tables 1 and 2). It is also obvious from the graphs that the North American euprimate polygons were larger in terms of area at every stratigraphic layer than were the European polygons. Second, these results suggest that a change in dietary and body size diversity took place during the Early to Middle Eocene transition in North America. A similar analysis could not be conducted for Europe due to a lack of information for taxa from speciﬁc stratigraphic layers, as well as a lack of certainty on the status of the stratigraphic layers themselves. To examine the relationship more closely between dietary and body size diversity, ecological distance, and time, regression analyses were performed on the average distance between taxa and the average distance from the centroid within an assemblage through time. Polygon area regressions were not performed because a maximum of only four points 244 C.C. GILBERT was available in North America, and no similar analysis was possible in Europe. It is worth noting, though, that all three measures are signiﬁcantly correlated with each other (area and average intertaxon distance: r ⫽ 0.671, p ⬍ 0.000; ⫽ 0.431, p ⫽ 0.004; area and average distance from centroid: r ⫽ 0.879, p ⬍ 0.000; ⫽ 0.605; p ⬍ 0.000; average intertaxon distance and average distance from centroid: r ⫽ 0.930, p ⬍ 0.000; ⫽ 0.819, p ⬍ 0.000). North American omomyoid primates’ average intertaxon distance was signiﬁcantly positively correlated with time, although the r2 value was low (r2 ⫽ 0.078, p ⫽ 0.001). Overall, the average intertaxon distance of North American euprimates was significantly positively correlated with time as well, and the r2 value was again quite low (r2 ⫽ 0.038, p ⫽ 0.014). Therefore, the results of the regression analysis suggest that while a signiﬁcant positive relationship between dietary/body size diversity and time existed within a biogeographic assemblage, time alone explained only a small portion of the variance. This makes good intuitive sense when one considers that many factors other than time are involved in the creation of new species and ecological niches. Geological events, climactic conditions, geographic features, and competition between individuals were all likely to play signiﬁcant roles as well. DISCUSSION This study reconstructed Eocene euprimate dietary and body size diversity in North America and Europe. Similar to extant primates (Fleagle and Reed, 1996), the results suggest that fossil euprimate ecological diversity during the Eocene epoch also differed signiﬁcantly between biogeographic areas. North American euprimates during the Early to Middle Eocene were signiﬁcantly more diverse in terms of body size and diet than European euprimates. Omomyoids in North America during this time were characterized by a large number of both frugivorous/gumnivorous and insectivorous taxa that were all under 500 g, except for Hemiacodon gracilis. This taxon had a positive shearing quotient, and probably included a signiﬁcant portion of leaves in its diet along with other food items (see also Gunnell and Rose, 2002). Omomyoids in Europe during the Early and Middle Eocene were much less speciose than their North American relatives, and were most likely all small (⬍500 g) insectivores. Adapoid primates in the Early and Middle Eocene of North America were all above 500 g in body mass, and many taxa were above 1,000 g. Along with an increase in body size, North American adapoids most likely shifted from a predominantly frugivorous diet in the Early Eocene to a more folivorous diet in the Middle Eocene (Covert, 1986). Meanwhile, European adapoid taxa during this time are both above and below the Kay’s 500-g threshold (1975, 1984), and their diet probably ranged from insectivorous to insectivorous/frugivorous to primarily frugivorous. Another interesting point illustrated by the graphs (Figs. 3– 6) concerns the relative position of the polygons representing the separate euprimate radiations. The polygons representing the two superfamilies, Adapoidea and Omomyoidea, were distinct from each other and never overlap in terms of dietary ecospace in North America at any time period sampled. This ﬁnding supports a recent suggestion by Gunnell (2002) that the North American adapoid and omomyoid radiations had distinct differences in the ecospace that they occupied. Previously, Fleagle (1978), Gingerich (1981), and Covert (1986) also noted that the two primate superfamilies appeared to be distinct in their body size distributions. Displacement between the superfamilies is probably best explained by competition between the two groups of similarly adapted, closely related animals (Fleagle, 1978). The results of this study also offer weak support to the notion that dietary and body size diversity and ecological distance between taxa increased through time as, presumably, the time since taxonomic divergence increased. In North America, there was a signiﬁcant positive correlation between time and the average intertaxon distance of the total euprimate polygons. However, the r2 value was quite low, and the only signiﬁcant difference detected between successive stratigraphic layers was between the Wa-6 and Wa-7 euprimate polygons in terms of average intertaxon distance (Fig. 5). Both omomyoid and adapoid taxa exhibited a trend towards increased body size through this time sequence, and most adapoid species along with one omomyoid species (H. gracilis) indicated a dietary shift to folivory. From these ﬁndings, further inferences can be drawn. If dietary and body size diversity is signiﬁcantly positively correlated with time, it follows that euprimates must have existed for a longer time on the continent of North America, in order to expand and occupy the greater amount of dietary ecospace observed. In addition, the euprimates of North America are clearly larger in body size than their European relatives (Figs. 3, 4), and a bias towards increased body size in an evolutionary lineage through time has been shown to exist, although the pattern is not consistent or ubiquitous for all primates (Heesy et al., unpublished ﬁndings). Stated more simply, the results may be used to suggest that euprimates had an earlier arrival on the continent of North America than on the continent of Europe. This suggestion, however, is only weakly supported by larger body sizes among North American euprimates and a low r2 value. Other explanations for the increased dietary and body size diversity observed in North America are probably more likely. There are certainly alternative ways to interpret the results of this study. One suggestion may be that EOCENE PRIMATE DIETARY DIVERSITY competition was simply more intense between primates and other mammalian groups during the Eocene of Europe, and that euprimates very quickly occupied the available niche space. Under this scenario, during the time period examined in this study, European euprimate assemblages could not subsequently expand in dietary ecospace from their original stronghold. In this light, the results of this study do not necessarily suggest an earlier divergence time for euprimates in North America, only that European euprimates occupied all available ecospace sooner than their North American relatives and did not expand signiﬁcantly in ecological diversity past that critical point. However, it is wellknown that during the early part of the Eocene, North America and Europe were connected by land bridges, and these connections allowed for faunal interchange to occur (McKenna, 1975; Russell, 1975; Fleagle, 1999). Faunal interchange between the two biogeographic areas would have allowed for similar fauna to be present in both regions (McKenna, 1975; Adams, 1981), and would suggest that primates were most likely in competition with similar groups of animals. It would, then, seem very odd that primates occupied such a signiﬁcantly larger portion of dietary niche space in North America than in Europe if they were in competition with relatives of the same groups of animals in both biogeographic areas. Here it could be pointed out that the MP-7 through MP-9 levels of the Early Eocene of Europe do not exactly correlate with the later Wasatchian of North America, and instead represent an earlier period of time. However, even the Wa-6 euprimate polygon, which does correlate closely to the upper border of the MP-8 through MP-9 levels of Europe (Lucas, 1998), has almost 2.5 times the area and a signiﬁcantly greater average intertaxon distance than the Early Eocene European euprimate polygon (Table 1). An important thing to remember when examining Eocene primate ecological diversity is that the depositional environment of France when compared to that of Wyoming is very different and may account for some of the large differences detected. Many fossil sites in France, rather than being a series of sediments laid down by a river ﬂowing through a basin, are best interpreted as karst ﬁllings resulting from Eocene tectonic faults (Astruc et al., 2000). As these karsts became exposed to the surface, they trapped ﬂora and fauna and were then ﬁlled with sediments that subsequently mineralized (Astruc et al., 2000). Therefore, they represent more of a random “snapshot” of the local fauna and may be less likely to truly preserve the total ecological diversity of primates from any one biogeographic area or time period. In addition, during the Middle Eocene of Western Europe, there was an expansion of the sea that divided and isolated the continent into a series of islands (Russell, 1975; Fleagle, 1999). This type of paleogeography would have effectively reduced the 245 area of land being sampled and therefore reduced the chances of sampling as many taxa in France as in Wyoming. A possible counterargument may be to suggest that islands are often biological “hotspots” of diversity, and so a more diverse fauna for the Middle Eocene of Europe should have been expected. The results of this study do not support such increased diversity in terms of diet and body size for the islands sampled in Western Europe vs. the western interior of North America. However, recent research suggests that ecological gradients can be more important than geographic isolation in the promotion of diversity (Schneider et al., 1999). This provides a possible explanation for the lower diversity observed in the isolated island refugia of Western Europe, especially during the Middle Eocene, and the increased diversity found instead in the more ecologically complex environments of North America (see discussion of basin margins, below). Another explanation for the apparent expansion of primate dietary and body size diversity in North America and the apparent lack of expansion observed in Europe during the Early to Middle Eocene involves the potential inﬂuence and effects of time averaging and sampling error. The gradual evolution of omomyoid and adapoid lineages during the Eocene of Wyoming is well-documented (e.g., Gingerich, 1979a, 1985; Bown and Rose, 1987). It is important to note, then, that when plotting taxa from North America, a single evolving lineage may be represented multiple times by a series of species. Therefore, taxa included on the plots may represent an earlier or later version of another taxon in the plot. This effect of time-averaging would have contributed some bias to measures of ecological diversity that are correlated with the number of taxa included. In fact, for all polygons (omomyoid polygons ⫹ adapoid polygons ⫹ combined euprimate polygons), the area of the polygon as well as the distance from the centroid were signiﬁcantly correlated with the number of taxa used in the analysis (r ⫽ 0.775, p ⬍ 0.000; r ⫽ 0.537, p ⫽ 0.007). When the polygons were analyzed separately by taxonomic group (Omomyoidea, Adapoidea, and combined euprimates), only one of the ecological measures (area of the euprimate polygons) was signiﬁcantly correlated with taxon number (r ⫽ 0.884, p ⫽ 0.004). Since the goal of the study was to represent a picture of overall diversity at any one point during the Early and Middle Eocene, it seemed appropriate to include as many taxa as possible, even if they only represented chronospecies of a single lineage. Even though some measures were correlated with taxon number, at no point was the average intertaxon distance of any set of polygons analyzed signiﬁcantly correlated with the number of taxa included in each polygon. Since this measure was signiﬁcantly greater in all North American euprimate polygons when compared to European euprimate polygons (Tables 1 and 2), it can be conﬁdently stated that the 246 C.C. GILBERT practice of including chronospecies did not obscure or bias the result that North American euprimate assemblages were indeed more diverse than their European counterparts. While keeping in mind the preceding caveats, it is hypothesized here that the main source of increased euprimate diversity sampled in North America during the Early and Middle Eocene has to do with the increased number of ecological niches and high rates of speciation provided by marginal environments found in Wyoming (Gunnell and Bartels, 2001a; Muldoon and Gunnell, 2002). Under evolutionary theory, populations isolated in peripheral or marginal areas can exhibit increased variability and speciation rates when compared to populations existing in more uniform environments, such as those in a basin center (Mayr, 1954; Smith et al., 1997; Kunin, 1998; Schneider et al., 1999). The South Pass fauna, in particular, is hypothesized by Gunnell and Bartels (2001a) as well as Muldoon and Gunnell (2002) to sample an ecologically diverse marginal environment with high levels of speciation and endemicity. Probable basin margin assemblages were documented for the Bighorn and Green River Basin as well (Gunnell, 1997; Gunnell and Bartels, 2001b). While the Bridgerian of the North American Middle Eocene was characterized by an inﬂux of omomyine taxa into the typically sampled lake margin and proximal ﬂoodplain environments, anaptomorphines were still common and diverse taxa out on the Bighorn and Green River basin margins (Gunnell, 1997). Therefore, the marginal environments of the western interior of North America preserved a large element of species and ecological diversity in addition to that usually sampled in a basin center. This degree of total basin diversity is not documented by environments in the Western European fossil record at this time. Whether this phenomenon is a result of real Early and Middle Eocene differences in rainforest habitats across the two biogeographic regions or an artifact of bias in the geological record of North America remains to be determined. However, the ecological gradients provided by marginal areas could have been more important than the geographic isolation provided by the Western European island refugia in the promotion of diversity (Schneider et al., 1999). A real biological phenomenon can therefore be invoked as an explanation for the increased diversity observed in North America, rather than a simple case of bias in the geological record. Clearer resolution of the differences between North American and European Eocene assemblages awaits future fossil discoveries and further studies documenting the structure of primate ecological diversity throughout the entire Eocene epoch rather than the small duration of time analyzed in this study. For example, as mentioned in the introduction, discoveries illuminating locomotor and activity patterns for the euprimate taxa analyzed here could alter our understanding of their ecological diversity. In addition, more studies detailing other portions of the Eocene will surely document different patterns in diversity, as euprimates become less common in the Late Eocene of North America but greatly diversify in the Late Eocene of Europe. CONCLUSIONS Two main conclusions were drawn from this study. 1) Euprimate dietary and body size diversity during the Early and Middle periods of the Eocene epoch differed signiﬁcantly among biogeographic areas. North American euprimates were signiﬁcantly more ecologically diverse in terms of dietary ecospace than their European counterparts at all times and by all measures. 2) Within biogeographic areas, dietary and body size diversity as characterized by average intertaxon distance expanded signiﬁcantly through time in North America. Euprimate taxa found in North America from the Middle Eocene were signiﬁcantly more distant on average than were those from the Early Eocene. Average intertaxon distance is signiﬁcantly positively correlated with time, although the relationship is weak. It is suggested that the differences in dietary and body size diversity observed between the euprimates of North America and the euprimates of Europe during the Early and Middle Eocene are most likely due in large part to the existence and sampling of more ecologically diverse environments, such as basin margins, in North America. ACKNOWLEDGMENTS I thank the following people for their help and encouragement during the duration of this study: John Fleagle, Theresa Franz, Biren Patel, the Norman Creel Prize Committee, and two anonymous reviewers for many helpful comments on previous drafts. I thank John Fleagle, Gregg Gunnell, Bill Jungers, David Krause, and Callum Ross for access to personal cast collections, use of equipment, assistance in securing museum visits, directions to important papers, and statistical advice. I thank the staff at the American Museum of Natural History, especially Chris Collins, Denny Diveley, and Bob Randall. I thank fellow graduate students, friends, and colleagues Summer Arrigo-Nelson, Jennifer Burns, Mark Coleman, Rob Fajardo, Meg Hall, Chris Heesy, Mitch Irwin, Keith Metzger, Anthony Olejniczak, Karen Samonds, Natasha Shah, Heather Smith, and Brandon Wheeler for help on various aspects of this paper and its associated presentations. Special thanks also go to Brandon Wheeler for software instruction and many thoughtful discussions throughout the course of this project. 247 EOCENE PRIMATE DIETARY DIVERSITY APPENDIX. M1 areas and SQ’s Adapoid taxon Early/Middle Eocene Biogeographic area M1 sample size (L, W) Source M1 area (mm2) Estimated body size (g) from Conroy, 1987 M2 sample size 2.26 21.12 53.84 1984.37 2 45 This study Covert, 1985 5.65 ⫺10.42 15.94 13.46 1260.44 958.79 43 2 Covert, 1985 This study ⫺6.89 ⫺19.86 11.52 3.50 34.10 23.29 3.59 1.87 29.92 26.74 746.42 109.07 4299.64 2324.24 113.63 39.66 3481.40 2903.62 60 X X 2 2 1 X 1 Covert, 1985 Generic average Generic average Covert, 1985 This study This study Generic average Covert, 1985 ⫺6.98 ⫺11.04 ⫺11.04 ⫺5.35 20.48 7.50 4.70 6.19 34.66 22.21 6.96 9.36 12.90 2.90 4414.87 2151.76 330.78 533.59 895.48 80.51 1 10 1 1 2 X This study Covert, 1985 This study This study This study Estimate from P. cirvicuspidens Estimate from P. cirvicuspidens Covert, 1985 Estimate from S. gracilis Anchomomys gaillardi Cantius abditus Middle Early Europe North America (2, 2) (1, 1) Cantius frugivorus Cantius mckennai Early Early North America North America (5, 5) (20, 19) Cantius ralstoni Cantius savagei Cantius simonsi Copelemur tutus Donrussellia gallica Donrussellia provinciallis Notharctus pugnax Notharctus robinsoni Early Early Early Early Early Early Middle Early/Middle North America Europe North America North America Europe Europe North America North America (16, 16) (1, 1) (1, 1) (4, 4) (3, 3) (3, 3) (6, 6) (2, 2) Notharctus robustior Notharctus tenebrosus Periconodon huerzeli Pronycticebus gaudryi Protoadapis curvicuspidens Protoadapis louisi Middle Middle Middle Middle Middle Early/Middle North America North America Europe Europe Europe Europe (50, 50) (20, 20) (5, 5) (1, 1) (2, 2) (1, 1) This study Gingerich and simons. 1977 Beard, 1988 Gingerich and Simons, 1977 Gingerich et al., 1982 Gingerich, 1977 Gunnell, 2002 Beard, 1988 This study Godinot, 1980 Gingerich, 1979b Gingerich, 1979b; Covert, 1985 Robinson, 1957 Gingerich et al., 1982 Godinot, 1988b This study This study Gingerich, 1977 Protoadapis russelli Early/Middle Europe (1, 1) Gingerich, 1977 2.50 63.36 X Smilodectes gracilis Smilodectes mcgrewi Middle Middle North America North America (37, 37) (3, 3) Covert, 1985 Glngerich, 1979b 13.89 20.00 1009.34 1817.31 10 X Absarokius abbotti Absarokius australis Absarokius gazini Absarokius metoecus Artimonius nocerai Early/Middle Early Early Early Early North North North North North 5.19 5.45 4.26 4.94 3.70 205.75 222.98 149.49 189.91 119.15 20 2 1 20 1 Anaptomorphus aemulus Anaptomorphus westi Middle Middle North America North America 4.26 6.31 149.49 282.43 Anemorhysis musculus Anemorhysis savagai Early Early North America North America 3.23 2.42 Anemorhysis sublettensis Early North America Anemorhysis wortmani Early North America Arapahovius gazini Aycrossia lovei Chlororhysis knightensis Hemiacodon gracilis Loveina minuta Early Middle Early Middle Early North North North North North Loveina zephyri Nannopihex ﬁlholi Nannopithex sp. Nannopithex zuccolae Omomys carteri Early Early/Middle Early Early/Middle Middle North America Europe Europe Europe North America Pseudoloris parvulus Shoshonius cooperi Middle Early Europe North America Steinius annectens Strigorhysis bridgerensis Trogolemur amplior Early Early/Middle Middle North America North America North America Trogolemur myodes Uintanius ameghini Uintanius rutherfordi Washakius insignis Early/Middle Middle Middle Middle North North North North Source SQ 5.26 2.65 ⫺9.64 6.50 ⫺2.00 ⫺2.00 ⫺2.00 7.14 7.14 Omomyoid taxon America America America America America America America America America America America America America America (130, 130) Bown and Rose, 1987 (2, 2) Bown and Rose, 1987 (3, 3) Bown and Rose, 1987 (50, 49) Bown and Rose, 1987 (2, 2) Bown and Rose, 1987; Muldoon and Gunnell, 2002 (2, 2) Gunnell, 1995 (7, 7) Gunnell, 1995; Muldoon and Gunnell, 2002 (1, 1) This study (8, 8) Williams and Covert, 1994 (1, 1) Bown and Rose, 1984; Williams and Covert, 1994 (2, 2) Bown and Rose, 1987; Williams and Covert, 1994 (2, 2) Bown and Rose, 1991 (1, 1) Bown and Rose, 1987 (2, 2) Gazin, 1962 (84, 84) Gunnell, 1995 (2, 2) This study; Bown and Rose, 1984 (2, 2) This study not given Conroy, 1987 (1, 1) This study (22, 22) Godinot et al., 1992 (5, 5) Bown and Rose, 1991; Muldoon and Gunnell, 2002 (7, 7) Godinot, 1988a (5, 5) Robinson, 1966; this study (1, 1) Bown and Rose, 1991 (3, 3) Bown and Rose, 1987 (2, 2) Gunnell, 1995; Beard et al., 1992 (7, 7) Gunnell, 1995 (1, 1) Gunnell, 1995 (1, 1) Robinson, 1966 (21, 21) Gunnell, 1995; Muldoon and Gunnell, 2002 X, no sample was available. The genetic average was used instead. ?, not given. Strait, Strait, Strait, Strait, Strait, 2001 2001 2001 2001 2001 7.28 4.86 ⫺8.71 11.89 1.95 2 1 Strait, 2001 Strait, 2001 2.97 0.34 95.81 60.20 1 X This study Generic average 2.15 49.49 1 Strait, 2001 4.54 3.08 88.73 2 Strait, 2001 11.26 4.51 5.16 3.66 10.66 2.85 164.21 204.07 116.97 658.44 78.30 6 6 1 3 1 15.52 ⫺9.22 ⫺5.50 5.17 28.76 3.67 3.39 5.18 3.35 5.40 117.92 103.45 205.35 101.62 219.79 1 1 1 X 20 Strait, 2001 Strait, 2001 This study This study This study; Strait, 2001 This study Strait, 2001 This study Generic average Strait, 2001 1.48 3.78 27.19 123.52 7 8 6.53 4.35 3.52 298.06 154.83 109.95 1 7 X 2.53 2.66 3.20 4.36 64.76 70.04 94.38 155.26 2 4 1 15 Strait, 2001 This study; Strait, 2001 Strait, 2001 Strait, 2001 Estimate from T. myodes Strait, 2001 Strait, 2001 This study Strait, 2001 ⫺9.49 2.10 ⫺5.99 9.70 33.47 21.58 18.37 17.90 15.47 9.14 21.91 ⫺13.72 ⫺13.72 25.61 4.00 ⫺21.30 248 C.C. 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