Acta Chiropterologica, 12(1): 143–154, 2010
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
doi: 10.3161/150811010X504644
Cranial differentiation of fruit-eating bats (genus Artibeus) based on
size-standardized data
MARÍA R. MARCHÁN-RIVADENEIRA1, 2, 5, CARLETON J. PHILLIPS1, RICHARD E. STRAUSS1,
JOSÉ ANTONIO GUERRERO3, CARLOS A. MANCINA4, and ROBERT J. BAKER1, 2
1Department
of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA
Natural Science Research Laboratory, Museum Texas Tech University Lubbock, TX 79409-3191, USA
3
Laboratorio de Sistemática y Morfología. Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos
Av. Universidad 1001, C.P. 62210, Cuernavaca, Morelos, México
4
División de Zoología, Instituto de Ecología y Sistemática, CITMA, Carretera de Varona, km 3 1/2, Capdevila, Boyeros,
Ciudad de La Habana, Cuba
5Corresponding author: raquel.marchan@ttu.edu
2
Size-standardized craniometric variation was investigated among species of the genus Artibeus. Eleven extant and one extinct
species were examined using geometric and linear morphometric analyses to evaluate morphological differences among species.
Based on 19 landmarks located in the ventral side of the cranium, 29 size-standardized linear measurements were calculated and
used for statistical multivariate analyses. Discriminant Function Analysis showed major interspecific differences in shape between
A. anthonyi and A. concolor with respect to the remaining extant species of Artibeus. These two species are described as
morphologically unique morphotypes with a broader rostrum, enlarged squamosal region, and wider basicranium. Specifically,
a broader premaxilla is the character that better discriminates A. anthonyi from all other species, whereas a broader squamosal region
(particularly the deep mandibular fossa, and elongated squamosal) and wider braincase are the main characters differentiating
A. concolor. All other species of the genus overlap to varying extents in their morphology showing high shape similarities. The least
variant shape features include the pterygoid fossa, the glenoid (mandibular) fossa, the maxillae, and the occipital region; these
regions in all cases contribute to mechanical aspects of jaw function and bite. The fact that the least variant aspects of skull shape
all involve feeding is consistent with the hypothesis that selection has favored a specific diet-associated morphology rather than
divergence or character displacement in Artibeus.
Key words: extinct and extant taxa, Neotropics, geometric and linear morphometrics
INTRODUCTION
More than 20% of all bat species occur in the
Neotropics. One of the most abundant are the fruiteating bats of the genus Artibeus, which are members of the subfamily Stenodermatinae — the most
diverse and recently evolved radiation of the New
World leaf nosed bats (Baker et al., 2003). This
genus is widely distributed from Mexico through
northern Argentina, including the Antillean islands
in the Caribbean (Simmons, 2005; Larsen et al.,
2007). Members of this genus play key roles in forest dynamics by dispersing seeds, mostly of figs
(one of the most species rich and habit-diverse
genera in the Neotropics — Harrison, 2005); promoting forest regeneration (Gorchov, 1993); and
contributing to the maintenance of floristic and
faunal diversity (Emmons and Feer, 1990). Because
of this, Artibeus has served as a model for several
studies in various fields such as ecology (Muscarella
and Fleming, 2007), conservation (Medellín et al.,
2000), behavioral analysis (Ortega et al., 2008), and
phylogeography (Larsen et al., 2007; Redondo et
al., 2008). However, all these studies have relied on
a still contentious taxonomy of the genus (Lim et al.,
2004; Larsen et al., 2007), which may provide a limited interpretation of results based on taxa relationships. Thus, a more thorough understanding of the
natural history of this genus and of its importance in
Neotropical ecosystems requires comprehensive
analyses of the variability among species to improve
the taxonomy of this group.
Traditionally, Artibeus (sensu lato) has been
split into two main groups based on body size. The
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M. R. Marchán-Rivadeneira, C. J. Phillips, R. E. Strauss, J. A. Guerrero, C. A. Mancina, et al.
smaller species of Artibeus have been classified in
the subgenus Dermanura and the larger ones in the
subgenus Artibeus (Artibeus sensu stricto). In addition, Owen (1987, 1991) proposed a new subgenus
named Koopmania to set apart one of the species,
A. concolor; however, this subgenus was later disregarded by Van Den Bussche et al. (1998) based on
morphological, karyotypic, enzymatic and molecular studies. Currently, extensive genetic data supports the hypothesis that Artibeus and Koopmania
represent a monophyletic assemblage of bats distinct from Dermanura (Van Den Bussche et al.,
1998; Hoofer et al., 2008; Solari et al., 2009). Herein, we follow the taxonomic classification proposed
by Hoofer et al. (2008) recognizing Artibeus distinct from Dermanura. Artibeus is comprised of 11
large-body size species including A. concolor as
the basal taxon. Additionally, the only known extinct
species in the genus is A. anthonyi (Wołoszyn
and Silva Taboada, 1977). Recently, Balseiro et al.
(2009) provided a detailed emended diagnosis of
A. anthonyi and a comprehensively morphometric
comparison with other extant species. However,
they did not include all the current extant taxa and
limited their study to an analysis of size variation
among species. Currently, species level taxonomy in
Artibeus is still under debate given the ample genetic and morphological variation, and wide distribution of the genus. Thus far, several molecular studies have explored the relationships among species,
but up-to-date morphological analyses that incorporate information on size and shape variation are
lacking and are needed to further characterize these
species.
Historically, species delimitation in Artibeus has
been studied using traditional morphological techniques (e.g., Patten, 1971; Marques-Aguiar, 1994;
Lim, 1997; Guerrero et al., 2003; Marchán-Rivadeneira, 2006, 2008; Balseiro et al., 2009), based
mostly on differences in size. Shape variation
among species has not been detailed. Analyses of
shape variation convey information on geometric
structure, which is more robust to allometric intraspecific differences (Zelditch et al., 2004) caused
by the dependence of shape upon size (Gould,
1966). This additional information also allows us to
understand the morphological variation in terms of
functional adaptations. For example, several authors
have shown that the configuration of the cranium
in the large species of Artibeus reflects an adaptive
response to consumption of hard fruits such as figs
(Kalko et al., 1996; Freeman, 1998; Dumont, 1999;
Swartz et al., 2003; Nogueira et al. 2009). These
adaptations include wide insertion of masticatory
muscles, wide palatal, short rostrum, deep dentarium, enlarged brain case, and well developed molars. In fact, the complex cranial morphology of
the species in this subgenus probably represents an
adaptive response to differences in feeding strategies. New studies that analyze cranial differences
in size and shape are expected to be particularly useful not only in clarifying species boundaries, but also
in the investigation of functional morphological
adaptations.
Our goal was to evaluate the morphological differences among species of Artibeus (extinct and
extant taxa) using geometric and linear morphometric techniques. We hypothesized that despite the
high similarity in skull morphology in this genus,
analyses of size-standardized skull measurements
can provide valuable information to differentiate the
species within Artibeus and insights about functional constraints. Specifically, we predicted that similarity in feeding strategies and resources consumed
among species will result in high morphological
similarity of cranial shape, assuming that morphological differences provide insights on the association of the morphological variation with feeding
habits. Here, we were focused on analyzing shape
configurations of the ventral side of the cranium
of all eleven extant species and the only known
extinct species (A. anthonyi). We used geometric
and linear morphometric analyses of 29 size-standardized linear measurements of the cranium calculated from 19 landmarks. Morphological differences
were contrasted with the currently accepted taxonomy and discussed in light of functional morphology.
MATERIALS AND METHODS
Specimens Examined
Seventy-five specimens of 11 extant and one extinct species
of the subgenus Artibeus were examined for this study (Fig. 1
and Appendix). Only adult specimens were included determined
by epyphyseal-diaphyseal fusion and reproductive condition
(Anthony, 1988) in extant species and toothwear in fossil specimens of the extinct A. anthonyi. In addition, five specimens of
Dermanura phaeotis (Appendix) were analyzed for comparison
because previous morphological and molecular studies agreed
that Dermanura is sister clade to Artibeus (Van Den Bussche et
al., 1998; Wetterer et al., 2000; Baker et al., 2003; Hoofer et al.,
2008; Redondo et al., 2008). In most cases, the specimens selected were collected close to the type locality of the species.
Landmark Data
Digitized images were obtained to analyze the configurations of 19 landmarks (Fig. 2A) on the ventral side of the
Cranial morphology in Artibeus
cranium. All images were digitized under standardized conditions and captured by the same person (i.e., MRMR, with
the exceptions of five of the seven specimens of A. anthonyi
which were photographed by CAM) to increase the precision
of data collection and to equally distribute digitizing errors
(Bogdanowicz, 2009). Images were obtained using an HP
Scanner 4070. Only the center lane of the scanner was used to
reduce differences in light distortion from the scanner bed
edges. Each cranium, resting on its dorsal surface, was laid on
modeling clay to avoid movement during image digitalization.
The scanner was turned upside down and placed over the skull
being digitized. A 50 mm separation was left from the table to
the scanner bed. The relative positions of landmarks were
digitized for each skull specimen with the TPS program series
(software modules developed by F. J. Rohlf, freely distributed at
http://life.bio.sunysb.edu/ morph/), which generated a matrix of
landmark coordinates used in all subsequent analyses. The landmarks selected were chosen to represent most of the variation in
the ventral side of the cranium. All landmarks were given equal
weight in distance calculations.
Statistical Analysis
The landmark coordinates matrix was used to estimate
a consensus form for each species. Initially, coordinates were
145
used to correct any residual bilateral asymmetry by reflection
and superimposition (Klingenberg et al., 2002). Altogether, this
procedure bilaterally reflects the form and maps it onto itself by
Procrustes superimposition, and returns the consensus configuration of landmarks. To avoid inflating degrees of freedom,
landmarks that were bilaterally homologous were averaged by
reflecting one side along a midline (defined by landmarks 1–5,
Fig. 2A).
The consensus forms were size-standardized for scaling size
variation by: 1) calculating all pairwise distances among landmarks; 2) regressing the log-transformed distances individually
on the first principal component scores (PC1, which accounted
for 98% of the variation in the sample, is a pooled within-group
PC1, not the overall PC1) of a principal component analysis of
the pairwise distances; and 3) substituting residuals, and refitting the landmark coordinates by multidimensional scaling
(Strauss and Marchán-Rivadeneira, unpublished). Then, using
the size-standardized coordinates, a Delaunay triangulation
was carried out to generate linear measurements based on the
largest number of triangles that satisfied this criterion (Small,
1996). This resulted in a total of 29 possible size-standardized linear distance measurements (Fig. 2B), named characters.
The log-transformed size-standardized distance data matrix
among the 29 characters was used for further ordination multivariate analyses.
FIG. 1. Collection localities of the specimens included in the morphometric analyses sorted by species. All Artibeus and Dermanura
specimens examined and localities are listed in Appendix. (M = A. amplus, = A. anthonyi, = A. concolor, = A. fimbriatus,
= A. fraterculus, = A. hirsutus, F = A. inopinatus, = A. jamaicensis, = A. lituratus, = A. obscurus, = A. planirostris,
$ = A. schwartzi, and M = D. phaeotis)
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M. R. Marchán-Rivadeneira, C. J. Phillips, R. E. Strauss, J. A. Guerrero, C. A. Mancina, et al.
The shape differences among species (n = 13) in the ventral
side of the cranium were assessed by size-standardized Discriminant Function Analysis (DFA) (dos Reis et al., 1990).
Corresponding size-invariant Mahalanobis distances among the
centroids of the species were calculated (dos Reis et al., 1990).
The percentage of correct classification by species was estimated based on a jackknifed cross-classification test. Shape changes
among species groups were visualized using the thin-plate
spline (Bookstein, 1989) based on size-standardized pairwise
consensus configurations of the 19 original landmarks described
on Fig. 2A. Because of the relatively small numbers of individuals per species, males and females of each species were pooled
for analysis. Any allometrically consistent size-variation between sexes was removed by the size-standardization procedures. Any non-allometric shape-variation between sexes was
still present as within-species variation, but is conservative because it serves to reduce discrimination among species.
To further explore shape variation in the assessment of the
phenetic relationships among the species shape, an Unweighted
Pair Group Method with Arithmetic Mean (UPGMA clustering
— Sneath and Sokal, 1973) clustering of Mahalanobis distances
was implemented. The cophenetic correlation and the rank
cophenetic coefficient were calculated as a measure of the
goodness of fit of the cluster analysis to the similarity matrix
(Rohlf, 1974). Also, the Gower similarity coefficient (sum of
squared-differences — see Gower, 1971) and mean squared difference were evaluated as measurements of proximity.
All statistical analyses were conducted using Matlab
version 6.5 (mainly using the library functions developed
by R. E. Strauss, freely available at http://www.faculty.biol.
ttu.edu/Strauss/Matlab/Matlab.htm). Alpha levels were predefined at 0.05 for each of the statistical values tested after 1,000
iterations.
RESULTS
Discriminant Function Analysis
For 80 specimens assigned to 13 independent
taxonomical groups, the size-standardized DFA partially discriminated all species (Fig. 3A). Still, due
to the overlap among most of the extant species
of Artibeus, excluding A. concolor, the percent of
correct assignment estimated based on minimum
Mahalanobis distances (among groups) was low
with only 54.7% of the total specimens correctly
classified to each of their initial morphological identifications after 1,000 iterations (Table 1).
The discriminant analysis identified nine useful
characters (15, 26, 29, 1, 7, 21, 6, 12, and 25;
A
B
FIG. 2. A — Positions of 19 landmark locations (black dots) on the ventral side of the cranium of A. jamaicensis (L-1: midpoint
between central incisors; L2: anterior limit of foramen magnum; L3: posterior end of the palatine; L4: midpoint of the extreme
curvature of the supraoccipital suture; L5: posterior limit of the foramen magnum; L6, 7: posterior margin of mastoid; L8, 9: most
anterior margin of mastoid; L10, 11: maximum curvature of the posterior margin of the zygomatic process; L12, 13: most anterior
point of the mandibular fossa along the zygomatic arch; L14, 15: tip of the palatal process; L16, 17: midpoint between M1 and M2;
L18, 19: midpoint between P1 and P2); B — Twenty-nine possible linear distance measurements (characters) among the 19 landmarks
obtained by Delaunay triangulation
Cranial morphology in Artibeus
arranged by contribution percent from high to low)
for the discrimination among species (Fig. 3B).
These discriminatory characters summarized patterns of differentiation among species in three cranial regions: 1) basioccipital region (distances 6, 7,
12, 15); 2) squamosal distance (distance 21); and 3)
palatal region (distances 1, 25, 26, 29). This differentiation was supported by a Multivariate analysis of variance (MANOVA) test (Wilks’ λ = 0.001,
F108, 45 = 6.71, P < 0.01).
The first discriminant function (DF1) accounted
for 77.5% of the variation in the sample, whereas the
DF2 accounted for 17% (see Table 2 for the contribution along the DF1 and DF2 of the 29 characters
employed). We identified three independent clusters
in DFA: D. phaeotis, A. concolor, and all the other
extant species of Artibeus (Fig. 3A). Artibeus anthonyi appeared along DF1 axis between A. concolor
and the other Artibeus extant species, overlapping
only partially with both of them. A vector plot of the
loadings of each character on DF1 (x-axis) and on
DF2 (y-axis) showed that D. phaeotis is distinguished from the entire Artibeus group mainly by
greater values in characters 9, 16, and 17 (Fig. 3B).
The discrimination among A. concolor and the rest
of the Artibeus group was primarily explained by its
greater values in characters 7 and 11 (Fig. 3B),
showing major deformations in the maxilla and
A
147
squamosal projection region in the ventral side of
the cranium (Fig. 4A). Artibeus anthonyi differed
from the extant species of Artibeus mainly by greater values in character 29 (Fig. 3B), showing major
deformations in the rostrum in the ventral side of the
cranium (Fig. 4B). Based on the median axis of DF2
(y = 0) the species comprising Artibeus can be
sorted in two groups that overlap only partially
(Fig. 3A). We identified these as group ‘A’ (concolor, inopinatus, fraterculus, jamaicensis, obscurus,
and lituratus), and group ‘B’ (amplus, anthonyi, fimbriatus, hirsutus, planirostris, and schwartzi).
Species in group A had all their specimens as well as
their centroids arranged above the median axis of
DF2 (with the only exceptions being a few specimens of A. jamaicensis and A. lituratus); whereas
species in group B had all their specimens and
centroids arranged under the median axis of DF2
(with the exception of only a few specimens of
A. amplus and A. anthonyi). Shape similarities for
species in group A were primarily in the basicranium region (characters 6, 7, 12, and 15 — Fig.
3B). On the other hand, shape similarities for species in group B involved mainly the palatal region,
maxilla, and pre-maxilla (characters 24, 25, 26, 27,
and 29 — Fig. 3B), showing major deformations in
the rostral region in the ventral side of the cranium
(Fig. 4C).
B
FIG. 3. A — Scatter plot of size-standardized DFA for all species of Artibeus and Dermanura examined (+ = species centroid).
B — Vector plot of the loadings on the first two discriminant functions (DF) showing the correlation between the 29 linear distance
measurements (characters) used in the analysis with each discriminant function. Complete lines represent the characters that
contributed more to the discrimination and that were identified as highly significant by the MANOVA (P < 0.01); dotted lines represent
non-significant characters. Numbers at the end of the arrows correspond to the linear measurements depicted in Fig. 2B
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M. R. Marchán-Rivadeneira, C. J. Phillips, R. E. Strauss, J. A. Guerrero, C. A. Mancina, et al.
TABLE 1. Results of a size-standardized DFA based on 29 linear
measurements (characters). Character numbers correspond to
linear measurements depicted in Fig. 2B. DF, discriminant
function; percent values refer to the % variation explained by
each DF
Character
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
DF1 (77.5%)
0.91
0.88
0.41
-0.33
0.11
0.60
-0.67
-0.80
-0.49
0.33
-0.36
0.26
-0.44
-0.12
0.81
-0.88
-0.88
-0.29
0.39
0.15
-0.03
0.16
0.34
-0.34
0.67
0.86
0.27
0.70
-0.12
DF2 (17.0%)
-0.07
-0.17
-0.37
0.20
-0.01
0.50
0.39
0.21
-0.09
0.19
0.32
0.25
0.18
0.07
0.50
-0.21
-0.26
0.14
-0.18
-0.14
-0.03
-0.19
-0.18
0.15
-0.26
-0.30
-0.17
-0.10
-0.50
Shape Similarity Analysis
The UPGMA based on size-standardized Mahalanobis distances (D2) summarized the similarities
in shape on the ventral side of the cranium among
the species examined (Fig. 5 and Table 1). The cluster analysis showed high morphological dissimilarity of D. phaeotis with respect to Artibeus species
(D2 ≥ 119.7 — Table 1) suggesting independence of
morphological features (100% support of 1,000
jackknife iterations), which was shown by DFA
(Fig 3). Two major conglomerates including Artibeus species were generated (clusters 1 and 2 —
Fig. 5). In terms of shape similarity, A. concolor was
grouped outside of the main cluster of the rest of
Artibeus species (dissimilarity supported in 100%
of 1,000 jackknife iterations), and it showed smaller
distances (D2 = 42.14 — Table 1) with respect to
A. anthonyi. The Mahalanobis distances matrix
showed high morphological similarities within Artibeus species included in cluster 1expressed by low
A
B
C
FIG. 4. Thin-plate spline showing the displacements of 19
landmarks (see Fig. 2A) used in the analyses from specific
consensus configurations of species of Artibeus examined. A —
Comparison of consensus form of species group A (black colour
line; A. concolor, A. inopinatus, A. fraterculus, A. jamaicensis,
A. obscurus, and A. lituratus) with consensus form of species
group B (gray colour line; A. amplus, A. anthonyi, A. fimbriatus,
A. hirsutus, A. planirostris, and A. schwartzi); B — Comparison
of consensus form of the extinct, A. anthonyi (black colour line),
with consensus form of extant species of Artibeus (gray colour
line; excluding A. concolor, see Discussion); C — Comparison
of consensus form of A. concolor (black colour line) with
consensus form of extant species of Artibeus (gray colour line)
distances values (between D2 = 2.40–63.76 — Table
1). Among these species, the extinct A. anthonyi was
morphologically more similar to A. amplus (D2 =
17.28) than to the rest of extant taxa of the cluster 1
(dissimilarity supported by 61% after 1,000 iterations). Morphological similarities within the extant
species in cluster 1 were not well supported (jackknife values ranged from 6 to 80%). For this analysis, the cophenetic and rank coefficient correlations were 0.98 and 0.88, respectively. The Gower
Cranial morphology in Artibeus
value was 127.32 and the mean squared difference
was 1.63.
DISCUSSION
The present study investigated the shape discrimination in the ventral side of the cranium among
extinct and extant species of Artibeus. Previous
studies of Artibeus showed differences in external
and craniodental characters that were useful for
discriminating among species using linear morphometric techniques (Patten, 1971; Marques-Aguiar,
1994; Lim, 1997; Guerrero et al., 2004; MarchánRivadeneira, 2006, 2008; Balseiro et al., 2009).
However, only a few of them used multivariate analyses, and all of them showed in some extent morphological overlap among the species studied (e.g.,
Lim, 1997; Guerrero et al., 2004; Marchán-Rivadeneira, 2006, 2008; Balseiro et al., 2009). The present study explored the utility of combined two dimensional multivariate analyses in extracting size
variation from the data matrix. Results from DFA
documented that species’ boundaries within Artibeus were partially distinguishable in shape configurations using geometric and linear morphometric
analyses on size-standardized data. Significantly,
149
this study found high morphological similarities
within Artibeus, and variants and invariants morphological features were used to characterize the
most discriminated groups of species. In this study,
interspecific differences in the ventral side of the
cranium were used to hypothesize ecomorphological implications of morphological differences.
Previous studies in bats showed that morphological
differences in structures located along the ventral
side of the cranium can be used to understand ecological features, such as differences in diet due to
morphological functional demands (e.g., SztencelJabłonka et al., 2009).
Results of DFA showed that the most noticeable differences occurred between A. anthonyi and
A. concolor in relation to all other species in Artibeus (Fig. 3), which overlapped to varying extents in
their morphology. The similarities among the species of Artibeus were further shown by the UPGMA
analysis. This analysis showed that the extant taxa of
Artibeus, with the exception of A. concolor, share
more similarities among themselves than with A. anthonyi (Fig. 5). We described Artibeus anthonyi and
A. concolor as morphometrically diagnosable species (Fig. 5). Comparisons of the displacements of
all 19 landmarks used showed that A. anthonyi and
FIG. 5. Dendrogram of UPGMA based on size-standardized Mahalanobis distances showing the shape similarities among extinct and
extant species of Artibeus. Support values obtained by the bootstrap analysis after 1,000 iterations are shown on the top of each branch
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M. R. Marchán-Rivadeneira, C. J. Phillips, R. E. Strauss, J. A. Guerrero, C. A. Mancina, et al.
TABLE 2. Percentage of correct classification by species (0 = 54.7%) estimated based on jackknife cross-classification test. Pairwise
Mahalanobis distances calculated among species of the genus Artibeus and Dermanura
Species
1
2
3
4
5
6
7
8
9
10
11
12
13
A. amplus
A. fimbriatus
A. fraterculus
A. hirsutus
A. inopinatus
A. jamaicensis
A. lituratus
A. obscurus
A. planirostris
A. schwartzi
A. anthonyi
A. concolor
D. phaeotis
Correct (%)
25.0
23.0
100.0
75.0
75.0
41.2
25.0
20.0
30.0
37.5
57.1
100.0
100.0
1
2
3
4
5
6
7
8
9
10
11
12
0
25.67
0
23.26 21.75
0
18.68
9.69 13.14
0
36.26 48.07 21.27 25.14
0
8.07 24.94
9.82 10.77 12.45
0
16.80 22.78 12.20 13.33 18.95
6.48
0
9.01 30.14
9.42 14.84 15.00
2.40 11.79
0
12.12 12.37 15.11
9.11 32.09
8.94
5.34 14.61
0
25.92 12.66 22.99 10.98 37.40 18.64
9.30 28.22
3.69
0
17.28 41.27 37.29 29.29 63.76 27.49 39.31 20.50 26.70 44.39
0
51.77 107.56 56.93 74.74 59.34 45.47 78.21 32.72 77.87 107.78 42.14
0
187.09 292.81 257.77 233.85 260.16 211.58 258.29 190.93 239.38 279.40 124.74 119.70
A. concolor differ from the other Artibeus by their
broader rostra (mostly the premaxillae, maxillae,
and palatine regions), enlarged squamosal region,
and wider basicranium (Fig. 4B−C). Specifically, a broader premaxilla is the character that best
discriminates A. anthonyi from all other species
(Fig. 3B — see also Balseiro et al., 2009), whereas
a broader squamosal region (particularly the deep
mandibular fossa, and elongated squamosal) and
wider braincase are the main characters differentiating A. concolor. We hypothesize that these differences might reflect different feeding strategies given
the role of the structures involved in masticatory
muscle support and jaw mechanics.
The broader premaxilla in A. anthonyi specimens
results in a wider gap between contralateral canine
teeth. Given the role of canine teeth in piercing and
holding fruit, the gap between contralateral teeth is
functionally important. In order to be effective, the
gap should be equal or less than the outside diameter of the fruit being eaten. Therefore, it is possible
that A. anthonyi fed on larger fruits than the typical
figs that constitute the dietary mainstay for most
extant species (August, 1981; Fleming, 1986; Handley, 1989; Giannini and Kalko, 2004). Whether the
average size of figs has changed over time, or Artibeus’ main diet resource has changed, or the diet of
A. anthonyi departed from that of extant Artibeus it
is not known.
On the other hand, the morphological uniqueness
of A. concolor associated with an elongated squamosal region, a deeper mandibular fossa, and
a wider braincase may reflect particular morphological associations with mastication considering the
role of these structures in this process. Previous
studies in bats including some species of Artibeus
show the association between size and shape of the
13
0
skull and diet (e.g., Freeman, 1998; Van Cakenberghe et al., 2002; Dumont, 2003). We could hypothesize that differences found in A. concolor
reflect some divergence in feeding mechanics and
diet resource used. Tandler et al. (1997) reported
that A. concolor has enzymes of submandibular salivary glands distinctly different from other Artibeus
species. Previous studies show that A. concolor is
mainly a frugivore canopy specialist, and also a folivore bat (Bernard, 1997, 2001) like other species
of the genus Artibeus (e.g., Gardner, 1977; Kunz
and Diaz, 1995). Additional studies are needed to
elucidate the functional association of changes in
size and shape of the cranium in A. concolor.
In this study, the determination of shape variants
allowed for the morphological recognition of two
species of Artibeus, which represent possible variations in skull morphology. This in turn implies that
the non-variant aspects of shape are actively constrained through selection. Identification of the constrained, or conserved, aspects of skull shape in
species of Artibeus sets the stage for understanding
selection forces. At the present time, it appears that
high morphological similarities among all species of
Artibeus limit our ability to determine species
boundaries on the basis of skull morphology, which
is dependent on a few shape characters that are allowed to fluctuate.
With the foregoing in mind, we also can ask
whether certain shape components are essentially
invariant among the Artibeus species. The least variant shape features are (not in order): the region including the pterygoid fossa; the glenoid (mandibular) fossa; the maxillae; and the occipital region.
These regions involve both posterior and anterior
bone developmental pathways, but in all cases contribute to mechanical aspects of jaw function and
Cranial morphology in Artibeus
bite. This is particularly true for the pterygoid fossae, the points of origin for the pterygoideus muscles, which insert laterally on the dentary, and the
glenoid fossa, where the dentary articulate with the
squamosal bone, contributing to mastication (Peigné
and De Bonis, 2003; Kemp, 2005). The stability in
the occipital region probably relates to the relationship between the skull and cervical vertebrae, which
in turn influences the angle of the head relative to
jaw opening and feeding. The fact that the least variant aspects of skull shape all involve feeding is consistent with the hypothesis that selection has favored
a specific diet-associated morphology rather than
divergence or character displacement in Artibeus.
Another finding of this study is that size-standardized DFA enabled the detection of two different
cranial regions of shape variation involved in defining morphological species boundaries in Artibeus.
The shape differences are mainly in the basicranium
and the palatal region (see Results). These regions
are related with different developmental and genetically independent ontogenetic pathways (Iseki et al.,
1999; Carter and Beaupré, 2001; Ornitz and Pierre,
2002; Opperman and Rawlins, 2005). Collectively
these components of the skull derived from the two
pathways are integrated to produce the adult skull
morphology. Previous studies showed that traits related by ontogeny or function have great influence
on each other and may form discrete groups called
modules (Olson and Miller, 1958). Porto et al. (2009)
found that modular structure in the skull of mammals is probably maintained by stabilizing selection
due to functional and developmental constraints,
which results in the maintenance of the overall integration structure and increasing of the modular
architecture of the skull (see also Marroig et al.,
2009). Modularity and developmental constraints of
bat skull have not been examined. Future studies for
assessing modules in skull morphology in Artibeus
will provide an understanding of how cranial modularity reflects specific functional or developmental
relationships among skull bones.
Taking what is known about basicranium and
palatal bone formation in the mammalian skull, we
can ask whether the two major discriminated groups
of Artibeus species reflect developmental constraints of the genus or some other aspect of the biology of these bats. When the species groupings
based on skull shape are compared to mtDNA-based
phylogenies (e.g., Lim et al., 2004; Larsen et al.,
2007; Hoofer et al., 2008; Redondo et al., 2008), it
is apparent that developmental origins of the shape
differences are not consistent, at least, with maternal
151
lineages. In fact, the developmental basis of shape
differences also appears to be independent of the
similarity tree based on morphological data (Fig. 5).
This is an important observation because it explains
the difficulty in identifying species of Artibeus
based on skull morphology and traditional taxonomic techniques.The absence of a geographic
pattern and the lack of congruence between the
developmental ‘type’ of shape differences and maternal lineages suggest that pathways to shape variation are independent of phylogenetic history
inferred from mitochondrial information. However,
the developmental pathways that produce the most
important shape differences in the skull might not be
randomly acquired within a lineage. If this is the
case, then the shape differences identified by the
present analyses might be products of selection.
In the future, sample size should be increased in
order to better evaluate the range of morphological
variation among widely distributed extant species
and to compare with the results present in this study.
Considering that most morphological structures are
three dimensional, future studies will be made to incorporate other skull views to analyze size and
shape within and among species. These data might
be used to evaluate the biological significance of
morphological features. Finally, variation of skull
morphology can be used to map morphological characters onto well-supported phylogenetic lineages to
determine the route of changes among the species.
This approach would contribute to a better understanding of the evolutionary relationships among the
species and correspondence with genetic relationships and ecological studies.
ACKNOWLEDGMENTS
This study was made possible by funding provided by the
Biological Database Program of Texas Tech University, the
Department of Biological Sciences at Texas Tech University, the
Museum of Texas Tech University, a Texas Public Education
Grant, and a Summer Thesis Dissertation Award from Texas
Tech University. The specimens listed in the Appendix are deposited at several museums, and we are greatly indebted to the
institutions, curators and staff for permission to examine specimens under their care, the use of their facilities, and their
hospitality. Thanks to (see names and acronyms of institutions
in Appendix): Nancy Simmons (AMNH), Eileen Westwig
(AMNH), Alfred Gardner (NMNH), Don E. Wilson (NMNH),
Linda K. Gordon (NMNH), Suzanne C. Peurach (NMNH), Jhon
R. Wible (CMNH), Sue McLaren (CMNH), and Carlos A. Mancina (CITMA).We thank Diego F. Alvarado, Rafael Escobar,
Peter A. Larsen, Sandra Yap, Alicia Daugherty, Burton Lim, and
Sergio Solari for reading a preliminary draft of this manuscript
and improving it. Reviews by two anonymous reviewers greatly improved the clarity of this paper.
152
M. R. Marchán-Rivadeneira, C. J. Phillips, R. E. Strauss, J. A. Guerrero, C. A. Mancina, et al.
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APPENDIX
Specimens examined. The 80 specimens included in morphometric analysis are housed in the following museum collections:
Museum of Texas Tech University, Lubbock (TTU); American Museum of Natural History, New York (AMNH); United States
National Museum, Smithsonian Institution (USNM); Carnegie Museum of Natural History (CMNH); and Colección Zoológica del
Instituto de Ecología y Sistemática, Ciudad de la Habana (CZACC) past Colección del Instituto de Zoología de la Academia de
Ciencias de Cuba (IZ)
Artibeus amplus (n = 4) ― Venezuela: Amazonas, Cerro
Duida, Cabecera Del Cano Culebra, 40 km NNW Esmeralda
(USNM 405343, 405344); Tamatama, Rio Orinoco (USNM
441470); Zulia, Kasmera, 21 km SW Machiques (USNM
440931).
A. anthonyi (n = 7) ― Cuba: Pinar del Rio, Viñales, Mogote
de la Guasasa, Cueva GEDA (CZACC 26.1933, 26.1936; Uncatalogued specimens 1, 2); Sancti Spiritus, Quarry in a limestone hill near Moza, 5 kms NE from Sancti Spiritus (CZACC
26. 1891 (IZ-344.5, Paratype)), Yaguajay, Loma de Judas,
Cueva Grande (CZACC 26.1911, 26.1912).
Artibeus concolor (n = 5) ― French Guiana: Cayenne, Sinnamary (AMNH 266269, 267193, 267195, 267477). Venezuela:
Amazonas, Rio Negro, Neblina Base Camp (AMNH 260014).
A. fimbriatus (n = 4) ― Brazil: Canindeyu, Igatimi (AMNH
234307); Guaira, Villarica (AMNH 217553); Parana, Salto
Grande (USNM 141390). Paraguay: locality unknown (USNM
105588).
A. fraterculus (n = 4) ― Ecuador: El Oro, Portovelo
(AMNH 47248); Cerro Chiche (TTU 102383); Zaruma,
El Faique (TTU 102753, 102756).
A. hirsutus (n = 4) ― Mexico: Jalisco, 2.5 Mi SW by Road
Atenquique (TTU 8700, 8701), 2.6 mi SW Atenquique, Cueva
Quemada (TTU 10594, 10595).
A. inopinatus (n = 4) ― Honduras: Valle, 6 km E Amatillo
(TTU 7685–7687, 7689).
A. jamaicensis (n = 16) ― Cuba: Guantanamo Province,
Guantanamo Bay Naval Station (TTU 52508, 52509, 52539,
52542–52546). Guatemala: Santa Rosa, Taxisco La Avellana
(AMNH 235316, 235318). Honduras: La Paz, El Manteado
(AMNH 126899); Tegucigalpa (AMNH 126209). Mexico:
Yucatan, Merida, Colonia Gineres, Villa Maria (TTU 18436);
19 km E Progreso (TTU 18437), San Antonio Teztiz, 4.7 mi S,
4.0 mi W Kinchil (TTU 18438, 18439).
A. lituratus (n = 4) ― Brazil: Minas Gerais, Vicosa (USNM
391094, 391096, 391097). Paraguay: Department Canindeyu,
Reserva Natural del Bosque M’Baracayu, 0.9 km E Headquarters (TTU 94040).
A. obscurus (n = 5) ― Bolivia: El Beni, Rio Cureraba, Beni
Reserve (USNM 564325), Rio Mattos, Beni Reserve near
Rancho Totaizal (USNM 564326); Santa Cruz, Parque Nacional
Kempff Mercado (USNM 584490, 584491). French Guiana:
Cayenne, Sinnamary (AMNH 266288).
A. planirostris (n = 10) ― Argentina: Jujuy, Yuto (AMNH
180303). Ecuador: Napo, Loreto, San Jose Nuevo (AMNH
67920). Grenada: St. George, Chemin R, 1/2 km E Confer
(CM 63322, 63324, 63329, 63330, 63332). Guyana: Hyde Park
(USNM 260028); Potoro Siparuni, Kato Kawa Valley (USNM
565533). St. Vincent and the Grenadines: Carriacou (CM
63370).
A. schwartzi (n = 8) ― St. Vincent and the Grenadines:
Carriacou (CM 63377, 63378), St. Vincent (CM 83208, 83210,
83212, 83213, 83221, 83224).
Dermanura phaeotis (n = 5) ― Costa Rica: Guanacaste,
10 Mi SW Canas, Rio Higueron (TTU 12976). El Salvador:
La Paz, 3 mi NW La Herradura (TTU 12987). Mexico: Guerrero, 24.1 mi N Rio La Union Hwy 200 (TTU 35544, 35546);
Nayarit, Rio Canas (TTU 33473).