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Dietary ecospace and the diversity of euprimates during the Early and Middle Eocene.

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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: cgilbert@ic.sunysb.edu
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. GILBERT
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