cranial differentiation of fruit-eating bats (genus ... · cranial differentiation of fruit-eating...

Acta Chiropterologica, 12(1): 143–154, 2010PL 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 2Natural Science Research Laboratory, Museum Texas Tech University Lubbock, TX 79409-3191, USA

3Laboratorio de Sistemática y Morfología. Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de MorelosAv. Universidad 1001, C.P. 62210, Cuernavaca, Morelos, México

4División de Zoología, Instituto de Ecología y Sistemática, CITMA, Carretera de Varona, km 3 1/2, Capdevila, Boyeros, Ciudad de La Habana, Cuba

5Corresponding author: [email protected]

Size-standardized craniometric variation was investigated among species of the genus Artibeus. Eleven extant and one extinctspecies 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 andused for statistical multivariate analyses. Discriminant Function Analysis showed major interspecific differences in shape betweenA. anthonyi and A. concolor with respect to the remaining extant species of Artibeus. These two species are described asmorphologically 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 leastvariant shape features include the pterygoid fossa, the glenoid (mandibular) fossa, the maxillae, and the occipital region; theseregions in all cases contribute to mechanical aspects of jaw function and bite. The fact that the least variant aspects of skull shapeall involve feeding is consistent with the hypothesis that selection has favored a specific diet-associated morphology rather thandivergence 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 theNeotropics. One of the most abundant are the fruit-eating bats of the genus Artibeus, which are mem-bers of the subfamily Stenodermatinae — the mostdiverse and recently evolved radiation of the NewWorld leaf nosed bats (Baker et al., 2003). Thisgenus is widely distributed from Mexico throughnorthern Argentina, including the Antillean islandsin the Caribbean (Simmons, 2005; Larsen et al.,2007). Members of this genus play key roles in for-est dynamics by dispersing seeds, mostly of figs(one of the most species rich and habit-diverse gen era in the Neotropics — Harrison, 2005); pro-moting forest regeneration (Gorchov, 1993); andcontributing to the maintenance of floristic and

faunal diversity (Emmons and Feer, 1990). Becauseof this, Artibeus has served as a model for severalstudies in various fields such as ecology (Muscarellaand Flem ing, 2007), conservation (Medellín et al.,2000), behavioral analysis (Ortega et al., 2008), andphylogeography (Larsen et al., 2007; Redondo etal., 2008). However, all these studies have relied ona still contentious taxonomy of the genus (Lim et al.,2004; Larsen et al., 2007), which may provide a lim-ited interpretation of results based on taxa relation-ships. Thus, a more thorough understanding of thenatural history of this genus and of its importance inNeotropical ecosystems requires comprehensiveanalyses of the variability among species to improvethe taxonomy of this group.

Traditionally, Artibeus (sensu lato) has been split into two main groups based on body size. The

144 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 inthe subgenus Dermanura and the larger ones in thesubgenus Artibeus (Artibeus sensu stricto). In addi-tion, Owen (1987, 1991) proposed a new subgenusnamed Koopmania to set apart one of the species, A. concolor; however, this subgenus was later disre-garded by Van Den Bussche et al. (1998) based onmorphological, karyotypic, enzymatic and molecu-lar studies. Currently, extensive genetic data sup-ports the hypothesis that Artibeus and Koopmaniarepresent a monophyletic assemblage of bats dis-tinct from Dermanura (Van Den Bussche et al.,1998; Hoofer et al., 2008; Solari et al., 2009). Here -in, we follow the taxonomic classification proposedby Hoofer et al. (2008) recognizing Artibeus dis-tinct from Dermanura. Artibeus is comprised of 11large-body size species including A. concolor as the basal taxon. Additionally, the only known extinctspecies 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 morphometriccomparison with other extant species. However,they did not include all the current extant taxa andlimited their study to an analysis of size variationamong species. Currently, species level taxonomy inArtibeus is still under debate given the ample genet-ic and morphological variation, and wide distribu-tion of the genus. Thus far, several molecular stud-ies have explored the relationships among species,but up-to-date morphological analyses that incorpo-rate information on size and shape variation arelacking and are needed to further characterize thesespecies.

Historically, species delimitation in Artibeus hasbeen studied using traditional morphological tech-niques (e.g., Patten, 1971; Marques-Aguiar, 1994;Lim, 1997; Guerrero et al., 2003; Marchán-Riva de -nei ra, 2006, 2008; Balseiro et al., 2009), basedmostly on differences in size. Shape variationamong species has not been detailed. Analyses ofshape variation convey information on geometricstructure, which is more robust to allometric in-traspecific differences (Zelditch et al., 2004) causedby the dependence of shape upon size (Gould,1966). This additional information also allows us tounderstand the morphological variation in terms offunctional adaptations. For example, several authorshave shown that the configuration of the cranium in the large species of Artibeus reflects an adaptiveresponse 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 masticatorymuscles, wide palatal, short rostrum, deep denta-rium, enlarged brain case, and well developed mo-lars. In fact, the complex cranial morphology of the spe cies in this subgenus probably represents anadaptive response to differences in feeding strate-gies. New studies that analyze cranial differences in size and shape are expected to be particularly use-ful not only in clarifying species boundaries, but alsoin the investigation of functional morphologicaladaptations.

Our goal was to evaluate the morphological dif-ferences among species of Artibeus (extinct and extant taxa) using geometric and linear morphomet-ric techniques. We hypothesized that despite thehigh similarity in skull morphology in this genus,analyses of size-standardized skull measurementscan provide valuable information to differentiate thespecies within Artibeus and insights about function-al constraints. Specifically, we predicted that simi-larity in feeding strategies and resources consumedamong species will result in high morphologicalsimilarity of cranial shape, assuming that morpho-logical differences provide insights on the asso-ciation of the morphological variation with feedinghabits. Here, we were focused on analyzing shapeconfigurations of the ventral side of the cranium of all eleven extant species and the only known extinct species (A. anthonyi). We used geometricand linear morphometric analyses of 29 size-stan-dardized linear measurements of the cranium calcu-lated from 19 landmarks. Morphological differenceswere contrasted with the currently accepted taxono-my and discussed in light of functional morphology.

MATERIALS AND METHODS

Specimens Examined

Seventy-five specimens of 11 extant and one extinct speciesof the subgenus Artibeus were examined for this study (Fig. 1and Appendix). Only adult specimens were included determinedby epyphyseal-diaphyseal fusion and reproductive condition(Anthony, 1988) in extant species and toothwear in fossil spec-imens of the extinct A. anthonyi. In addition, five specimens ofDermanura phaeotis (Appendix) were analyzed for comparisonbecause previous morphological and molecular studies agreedthat Dermanura is sister clade to Artibeus (Van Den Bussche etal., 1998; Wetterer et al., 2000; Baker et al., 2003; Hoofer et al.,2008; Redondo et al., 2008). In most cases, the specimens se-lected were collected close to the type locality of the species.

Landmark Data

Digitized images were obtained to analyze the config-urations of 19 landmarks (Fig. 2A) on the ventral side of the

FIG. 1. Collection localities of the specimens included in the morphometric analyses sorted by species. All Artibeus and Dermanuraspecimens 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)

Cranial morphology in Artibeus 145

cranium. All images were digitized under standardized condi-tions and captured by the same person (i.e., MRMR, with the exceptions of five of the seven specimens of A. anthonyiwhich were photographed by CAM) to increase the precision of data collection and to equally distribute digitizing errors(Bogdanowicz, 2009). Images were obtained using an HPScanner 4070. Only the center lane of the scanner was used toreduce differences in light distortion from the scanner bededges. Each cranium, resting on its dorsal surface, was laid onmodeling clay to avoid mov e ment during image digitalization.The scanner was turned upside down and placed over the skullbeing digitized. A 50 mm separation was left from the table tothe scanner bed. The rel ative posi tions of landmarks weredigitized for each skull speci men with the TPS program series(software modules developed by F. J. Rohlf, freely distributed athttp://life.bio.sunysb.edu/ morph/), which generated a matrix oflandmark coordinates used in all subsequent analyses. The land-marks selected were chosen to represent most of the variation inthe ventral side of the cranium. All landmarks were given equalweight in distance calculations.

Statistical Analysis

The landmark coordinates matrix was used to estimate a con sensus form for each species. Initially, coordinates were

used to correct any residual bilateral asymmetry by reflectionand superimposition (Klingenberg et al., 2002). Altogether, thisprocedure bilaterally reflects the form and maps it onto itself byProcrustes superimposition, and returns the consensus configu-ration of landmarks. To avoid inflating degrees of freedom,land marks that were bilaterally homologous were averaged byreflecting one side along a midline (defined by landmarks 1–5,Fig. 2A).

The consensus forms were size-standardized for scaling sizevariation by: 1) calculating all pairwise distances among land-marks; 2) regressing the log-transformed distances individuallyon the first principal component scores (PC1, which accountedfor 98% of the variation in the sample, is a pooled within-groupPC1, not the overall PC1) of a principal component analysis ofthe pairwise distances; and 3) substituting residuals, and refit-ting the landmark coordinates by multidimensional scaling(Strauss and Marchán-Rivadeneira, unpublished). Then, usingthe size-standardized coordinates, a Delaunay triangulation was carried out to generate linear measurements based on thelargest number of triangles that satisfied this criterion (Small,1996). This resulted in a total of 29 possible size-standard-ized linear distance measurements (Fig. 2B), named characters.The log-transformed size-standardized distance data matrixamong the 29 characters was used for further ordination multi-variate analyses.

FIG. 2. A — Positions of 19 landmark locations (black dots) on the ventral side of the cranium of A. jamaicensis (L-1: midpointbetween central incisors; L2: anterior limit of foramen magnum; L3: posterior end of the palatine; L4: midpoint of the extremecurvature of the supraoccipital suture; L5: posterior limit of the foramen magnum; L6, 7: posterior margin of mastoid; L8, 9: mostanterior margin of mastoid; L10, 11: maximum curvature of the posterior margin of the zygomatic process; L12, 13: most anteriorpoint 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

A B

The shape differences among species (n = 13) in the ventralside of the cranium were assessed by size-standardized Dis -criminant Function Analysis (DFA) (dos Reis et al., 1990).Corresponding size-invariant Mahalanobis distances among thecentroids of the species were calculated (dos Reis et al., 1990).The percentage of correct classification by species was estimat-ed based on a jackknifed cross-classification test. Shape changesamong species groups were visualized using the thin-platespline (Bookstein, 1989) based on size-standardized pairwiseconsensus configurations of the 19 original landmarks describedon Fig. 2A. Because of the relatively small numbers of individ-uals per species, males and females of each species were pooledfor analysis. Any allometrically consistent size-variation be-tween sexes was removed by the size-standardization proce-dures. Any non-allometric shape-variation between sexes wasstill present as within-species variation, but is conservative be-cause it serves to reduce discrimination among species.

To further explore shape variation in the assessment of thephenetic relationships among the species shape, an UnweightedPair Group Method with Arithmetic Mean (UPGMA clustering— Sneath and Sokal, 1973) clustering of Mahalanobis distanceswas implemented. The cophenetic correlation and the rankcophenetic 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 ofsquared-differences — see Gower, 1971) and mean squared dif-ference 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 prede-fined at 0.05 for each of the statistical values tested after 1,000iterations.

RESULTS

Discriminant Function Analysis

For 80 specimens assigned to 13 independenttax on omical groups, the size-standardized DFA par-tially discriminated all species (Fig. 3A). Still, dueto the overlap among most of the extant species of Artibeus, excluding A. concolor, the percent of correct assignment estimated based on minimumMahalanobis distances (among groups) was lowwith only 54.7% of the total specimens correctlyclassified to each of their initial morphological iden-tifications after 1,000 iterations (Table 1).

The discriminant analysis identified nine usefulcharacters (15, 26, 29, 1, 7, 21, 6, 12, and 25;


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 distancemeasurements (characters) used in the analysis with each discriminant function. Complete lines represent the characters thatcontributed 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


ar ranged by contribution percent from high to low)for the discrimination among species (Fig. 3B).These discriminatory characters summarized pat-terns of differentiation among species in three cra -nial regions: 1) basioccipital region (distances 6, 7,12, 15); 2) squamosal distance (distance 21); and 3)palatal region (distances 1, 25, 26, 29). This dif-ferentiation was supported by a Multivariate analy-sis of variance (MANOVA) test (Wilks’ λ = 0.001, F108, 45 = 6.71, P < 0.01).

The first discriminant function (DF1) accountedfor 77.5% of the variation in the sample, whereas theDF2 accounted for 17% (see Table 2 for the contri-bution along the DF1 and DF2 of the 29 charactersemployed). We identified three independent clustersin DFA: D. phaeotis, A. concolor, and all the otherextant species of Artibeus (Fig. 3A). Artibeus antho-nyi appeared along DF1 axis between A. concolorand the other Artibeus extant species, overlappingonly partially with both of them. A vector plot of theloadings of each character on DF1 (x-axis) and onDF2 (y-axis) showed that D. phaeotis is distin-guished from the entire Artibeus group mainly bygreater values in characters 9, 16, and 17 (Fig. 3B).The discrimination among A. concolor and the restof the Artibeus group was primarily explained by itsgreater values in characters 7 and 11 (Fig. 3B),show ing major deformations in the maxilla and

squamosal projection region in the ventral side ofthe cranium (Fig. 4A). Artibeus anthonyi differedfrom the extant species of Artibeus mainly by great -er values in character 29 (Fig. 3B), showing majordeformations in the rostrum in the ventral side of thecranium (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’ (conco-lor, inopinatus, fraterculus, jamaicensis, obscurus,and lituratus), and group ‘B’ (amplus, anthonyi, fim-briatus, hirsutus, planirostris, and schwartzi).Species in group A had all their specimens as well astheir centroids arranged above the median axis ofDF2 (with the only exceptions being a few speci-mens of A. jamaicensis and A. lituratus); whereasspecies in group B had all their specimens and centroids arranged under the median axis of DF2(with the exception of only a few specimens ofA. amplus and A. anthonyi). Shape similarities forspecies in group A were primarily in the basi-cranium region (characters 6, 7, 12, and 15 — Fig.3B). On the other hand, shape similarities for spe -cies 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).

A B

FIG. 4. Thin-plate spline showing the displacements of 19landmarks (see Fig. 2A) used in the analyses from specificconsensus configurations of species of Artibeus examined. A —Comparison of consensus form of species group A (black colourline; A. concolor, A. inopinatus, A. fraterculus, A. jamaicensis,A. obscurus, and A. lituratus) with consensus form of speciesgroup B (gray colour line; A. amplus, A. anthonyi, A. fimbriatus,A. hirsutus, A. planirostris, and A. schwartzi); B — Comparisonof consensus form of the extinct, A. anthonyi (black colour line),with consensus form of extant species of Artibeus (gray colourline; excluding A. concolor, see Discussion); C — Comparisonof consensus form of A. concolor (black colour line) withconsensus form of extant species of Artibeus (gray colour line)

distances values (between D2 = 2.40–63.76 — Table1). Among these species, the extinct A. anthonyi wasmorphologically 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 itera-tions). Morphological similarities within the extantspecies in cluster 1 were not well supported (jack-knife values ranged from 6 to 80%). For this anal-ysis, the cophenetic and rank coefficient correla-tions were 0.98 and 0.88, respectively. The Gower

A

B

C


Shape Similarity Analysis

The UPGMA based on size-standardized Ma -halanobis distances (D2) summarized the similaritiesin shape on the ventral side of the cranium amongthe species examined (Fig. 5 and Table 1). The clus-ter analysis showed high morphological dissimilari-ty of D. phaeotis with respect to Artibeus species(D2 ≥ 119.7 — Table 1) suggesting independence ofmorphological features (100% support of 1,000jackknife iterations), which was shown by DFA (Fig 3). Two major conglomerates including Ar -tibeus species were generated (clusters 1 and 2 —Fig. 5). In terms of shape similarity, A. concolor wasgrouped outside of the main cluster of the rest ofArtibeus species (dissimilarity supported in 100% of 1,000 jackknife iterations), and it showed smallerdistances (D2 = 42.14 — Table 1) with respect to A. an thonyi. The Mahalanobis distances matrixshow ed high morphological similarities within Arti -beus species included in cluster 1expressed by low

TABLE 1. Results of a size-standardized DFA based on 29 linearmeasurements (characters). Char acter numbers correspond tolinear measurements depicted in Fig. 2B. DF, discriminant function; percent values refer to the % variation explained byeach DF

Character DF1 (77.5%) DF2 (17.0%)

1 0.91 -0.072 0.88 -0.173 0.41 -0.374 -0.33 0.205 0.11 -0.016 0.60 0.507 -0.67 0.398 -0.80 0.219 -0.49 -0.09

10 0.33 0.1911 -0.36 0.3212 0.26 0.2513 -0.44 0.1814 -0.12 0.0715 0.81 0.5016 -0.88 -0.2117 -0.88 -0.2618 -0.29 0.1419 0.39 -0.1820 0.15 -0.1421 -0.03 -0.0322 0.16 -0.1923 0.34 -0.1824 -0.34 0.1525 0.67 -0.2626 0.86 -0.3027 0.27 -0.1728 0.70 -0.1029 -0.12 -0.50

FIG. 5. Dendrogram of UPGMA based on size-standardized Mahalanobis distances showing the shape similarities among extinct andextant species of Artibeus. Support values obtained by the bootstrap analysis after 1,000 iterations are shown on the top of each branch


value was 127.32 and the mean squared differencewas 1.63.

DISCUSSION

The present study investigated the shape discrim-ination in the ventral side of the cranium among extinct and extant species of Artibeus. Previousstudies of Artibeus showed differences in externaland craniodental characters that were useful for discriminating among species using linear morpho-metric techniques (Patten, 1971; Marques-Aguiar,1994; Lim, 1997; Guerrero et al., 2004; Marchán-Rivadeneira, 2006, 2008; Balseiro et al., 2009).However, only a few of them used multivariate anal -yses, and all of them showed in some extent mor-phological overlap among the species studied (e.g.,Lim, 1997; Gu er rero et al., 2004; Marchán-Riva -deneira, 2006, 2008; Balseiro et al., 2009). The pres-ent study explored the utility of combined two di-mensional multivariate analyses in extracting sizevariation from the data matrix. Results from DFAdocumented that species’ boundaries within Art i -beus were partially distinguishable in shape config-urations using geometric and linear morphometricanalyses on size-standardized data. Significantly,

this study found high morphological similaritieswithin Artibeus, and variants and invariants mor-phological features were used to characterize themost discriminated groups of species. In this study,interspecific differences in the ventral side of thecranium were used to hypothesize ecomorpholog-ical implications of morphological differences.Previous studies in bats show ed that morphologicaldifferences in structures located along the ventralside of the cranium can be used to understand eco-logical features, such as differences in diet due tomorphological functional demands (e.g., Sztencel-Jabłonka et al., 2009).

Results of DFA showed that the most notice-able differences occurred between A. anthonyi andA. con color in relation to all other species in Arti -beus (Fig. 3), which overlapped to varying extents intheir morphology. The similarities among the spe -cies of Artibeus were further shown by the UPGMAanalysis. This analysis showed that the extant taxa ofArtibeus, with the exception of A. concolor, sharemore similarities among themselves than with A. an-thonyi (Fig. 5). We described Artibeus anthonyi andA. concolor as morphometrically diagnosable spe -cies (Fig. 5). Comparisons of the displacements ofall 19 landmarks used showed that A. anthonyi and


A. concolor differ from the other Artibeus by theirbroader rostra (mostly the premaxillae, maxillae,and palatine regions), enlarged squamosal region,and wider basicranium (Fig. 4B−C). Specifical-ly, a broader premaxilla is the character that bestdiscriminates A. anthonyi from all other species(Fig. 3B — see also Balseiro et al., 2009), whereasa broader squamosal region (particularly the deepmandibular fossa, and elongated squamosal) andwider braincase are the main characters differentiat-ing A. concolor. We hypothesize that these differ-ences might reflect different feeding strategies giventhe role of the structures involved in masticatorymuscle support and jaw mechanics.

The broader premaxilla in A. anthonyi specimensresults in a wider gap between contralateral canineteeth. Given the role of canine teeth in piercing andholding fruit, the gap between contralateral teeth isfunctionally important. In order to be effective, thegap should be equal or less than the outside diame-ter of the fruit being eaten. Therefore, it is possiblethat A. anthonyi fed on larger fruits than the typicalfigs that constitute the dietary mainstay for most extant species (August, 1981; Fleming, 1986; Hand -ley, 1989; Giannini and Kalko, 2004). Whether theaverage size of figs has changed over time, or Arti -beus’ main diet resource has changed, or the diet ofA. anthonyi departed from that of extant Artibeus itis not known.

On the other hand, the morphological uniquenessof A. concolor associated with an elongated squa -mo sal region, a deeper mandibular fossa, and a wider braincase may reflect particular morpholog-ical associations with mastication considering therole of these structures in this process. Previousstudies in bats including some species of Artibeusshow the association between size and shape of the

skull and diet (e.g., Freeman, 1998; Van Caken -berghe et al., 2002; Dumont, 2003). We could hy -pothesize that differences found in A. concolorreflect some divergence in feeding mechanics anddiet resource used. Tandler et al. (1997) reportedthat A. concolor has enzymes of submandibular sali-vary glands distinctly different from other Artibeusspe cies. Previous studies show that A. concolor ismainly a frugivore canopy specialist, and also a fo-livore bat (Bernard, 1997, 2001) like other speciesof the genus Artibeus (e.g., Gardner, 1977; Kunzand Diaz, 1995). Additional studies are needed toelucidate the functional association of changes insize and shape of the cranium in A. concolor.

In this study, the determination of shape variantsallowed for the morphological recognition of twospecies of Artibeus, which represent possible varia-tions in skull morphology. This in turn implies thatthe non-variant aspects of shape are actively con-strained through selection. Identification of the con-strained, or conserved, aspects of skull shape inspecies of Artibeus sets the stage for understandingselection forces. At the present time, it appears thathigh morphological similarities among all species ofArtibeus limit our ability to determine speciesbound aries on the basis of skull morphology, whichis dependent on a few shape characters that are al-lowed to fluctuate.

With the foregoing in mind, we also can askwhether certain shape components are essentiallyinvariant among the Artibeus species. The least vari-ant shape features are (not in order): the region in-cluding the pterygoid fossa; the glenoid (mandibu-lar) fossa; the maxillae; and the occipital region.These regions involve both posterior and anteriorbone developmental pathways, but in all cases con-tribute to mechanical aspects of jaw function and

TABLE 2. Percentage of correct classification by species (0 = 54.7%) estimated based on jackknife cross-classification test. PairwiseMahalanobis distances calculated among species of the genus Artibeus and Dermanura

Species Correct (%) 1 2 3 4 5 6 7 8 9 10 11 12 13

1 A. amplus 25.0 02 A. fimbriatus 23.0 25.67 03 A. fraterculus 100.0 23.26 21.75 04 A. hirsutus 75.0 18.68 9.69 13.14 05 A. inopinatus 75.0 36.26 48.07 21.27 25.14 06 A. jamaicensis 41.2 8.07 24.94 9.82 10.77 12.45 07 A. lituratus 25.0 16.80 22.78 12.20 13.33 18.95 6.48 08 A. obscurus 20.0 9.01 30.14 9.42 14.84 15.00 2.40 11.79 09 A. planirostris 30.0 12.12 12.37 15.11 9.11 32.09 8.94 5.34 14.61 0

10 A. schwartzi 37.5 25.92 12.66 22.99 10.98 37.40 18.64 9.30 28.22 3.69 011 A. anthonyi 57.1 17.28 41.27 37.29 29.29 63.76 27.49 39.31 20.50 26.70 44.39 012 A. concolor 100.0 51.77 107.56 56.93 74.74 59.34 45.47 78.21 32.72 77.87 107.78 42.14 013 D. phaeotis 100.0 187.09 292.81 257.77 233.85 260.16 211.58 258.29 190.93 239.38 279.40 124.74 119.70 0


bite. This is particularly true for the pterygoid fos-sae, the points of origin for the pterygoideus mus-cles, which insert laterally on the dentary, and theglenoid fossa, where the dentary articulate with thesqua mosal bone, contributing to mastication (Peignéand De Bonis, 2003; Kemp, 2005). The stability inthe occipital region probably relates to the relation-ship between the skull and cervical vertebrae, whichin turn influences the angle of the head relative tojaw opening and feeding. The fact that the least vari-ant aspects of skull shape all involve feeding is con-sistent with the hypothesis that selection has favoreda specific diet-associated morphology rather than divergence or character displacement in Artibeus.

Another finding of this study is that size-stan-dardized DFA enabled the detection of two differentcranial regions of shape variation involved in defin-ing morphological species boundaries in Artibeus.The shape differences are mainly in the basicraniumand the palatal region (see Results). These regionsare related with different developmental and geneti-cally independent ontogenetic pathways (Iseki et al.,1999; Carter and Beaupré, 2001; Ornitz and Pierre,2002; Opperman and Rawlins, 2005). Collectivelythese components of the skull derived from the twopathways are integrated to produce the adult skullmorphology. Previous studies showed that traits re-lated by ontogeny or function have great influenceon each other and may form discrete groups calledmodules (Olson and Miller, 1958). Porto et al. (2009)found that modular structure in the skull of mam-mals is probably maintained by stabilizing selectiondue to functional and developmental constraints,which results in the maintenance of the overall inte-gration structure and increasing of the modular architecture of the skull (see also Marroig et al.,2009). Modularity and developmental constraints ofbat skull have not been examined. Future studies forassessing modules in skull morphology in Artibeuswill provide an understanding of how cranial modu-larity reflects specific functional or developmentalrelationships among skull bones.

Taking what is known about basicranium andpalatal bone formation in the mammalian skull, wecan ask whether the two major discriminated groupsof Artibeus species reflect developmental con-straints of the genus or some other aspect of the bi-ology of these bats. When the species groupingsbased on skull shape are compared to mtDNA-basedphylogenies (e.g., Lim et al., 2004; Larsen et al.,2007; Hoofer et al., 2008; Redondo et al., 2008), itis apparent that developmental origins of the shapedifferences are not consistent, at least, with maternal

lineages. In fact, the developmental basis of shapedifferences also appears to be independent of thesimilarity tree based on morphological data (Fig. 5).This is an important observation because it explainsthe difficulty in identifying species of Artibeusbased on skull morphology and traditional taxo-nomic techniques.The absence of a geographic pattern and the lack of congruence between the developmental ‘type’ of shape differences and ma-ternal lineages suggest that pathways to shape vari-ation are independent of phylogenetic history in ferred from mitochondrial information. However,the developmental pathways that produce the mostimportant shape differences in the skull might not berandomly acquired within a lineage. If this is thecase, then the shape differences identified by thepresent analyses might be products of selection.

In the future, sample size should be increased inorder to better evaluate the range of morphologicalvariation among widely distributed extant speciesand to compare with the results present in this study.Considering that most morphological structures arethree dimensional, future studies will be made to in-corporate other skull views to analyze size andshape within and among species. These data mightbe used to evaluate the biological significance ofmorphological features. Finally, variation of skullmorphology can be used to map morphological cha -racters onto well-supported phylogenetic lineages todetermine the route of changes among the species.This approach would contribute to a better under-standing of the evolutionary relationships among thespecies and correspondence with genetic relation-ships and ecological studies.

ACKNOWLEDGMENTS

This study was made possible by funding provided by theBiological Database Program of Texas Tech University, theDepartment of Biological Sciences at Texas Tech University, theMuseum of Texas Tech University, a Texas Public EducationGrant, and a Summer Thesis Dissertation Award from TexasTech University. The specimens listed in the Appendix are de-posited at several museums, and we are greatly indebted to theinstitutions, curators and staff for permission to examine speci-mens under their care, the use of their facilities, and their hospitality. Thanks to (see names and acronyms of institutionsin Appendix): Nancy Simmons (AMNH), Eileen Westwig(AMNH), Alfred Gardner (NMNH), Don E. Wilson (NMNH),Linda K. Gordon (NMNH), Suzanne C. Peurach (NMNH), JhonR. Wible (CMNH), Sue McLaren (CMNH), and Carlos A. Man -cina (CITMA).We thank Diego F. Alvarado, Rafael Escobar,Peter A. Larsen, Sandra Yap, Alicia Daugherty, Burton Lim, andSergio Solari for reading a preliminary draft of this manuscriptand improving it. Reviews by two anonymous reviewers great-ly improved the clarity of this paper.


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Received 02 October 2009, accepted 02 April 2010


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 StatesNational Museum, Smithsonian Institution (USNM); Carnegie Museum of Natural History (CMNH); and Colección Zoológica delInstituto de Ecología y Sistemática, Ciudad de la Habana (CZACC) past Colección del Instituto de Zoología de la Academia deCiencias de Cuba (IZ)

Artibeus amplus (n = 4) ― Venezuela: Amazonas, CerroDuida, Cabecera Del Cano Culebra, 40 km NNW Esmeralda(USNM 405343, 405344); Tamatama, Rio Orinoco (USNM441470); Zulia, Kasmera, 21 km SW Machiques (USNM440931).

A. anthonyi (n = 7) ― Cuba: Pinar del Rio, Viñales, Mogotede la Guasasa, Cueva GEDA (CZACC 26.1933, 26.1936; Un -catalogued specimens 1, 2); Sancti Spiritus, Quarry in a lime-stone hill near Moza, 5 kms NE from Sancti Spiritus (CZACC26. 1891 (IZ-344.5, Paratype)), Yaguajay, Loma de Judas,Cueva Grande (CZACC 26.1911, 26.1912).

Artibeus concolor (n = 5) ― French Guiana: Cayenne, Sin -namary (AMNH 266269, 267193, 267195, 267477). Vene zu ela:Amazonas, Rio Negro, Neblina Base Camp (AMNH 260014).

A. fimbriatus (n = 4) ― Brazil: Canindeyu, Igatimi (AMNH234307); Guaira, Villarica (AMNH 217553); Parana, SaltoGrande (USNM 141390). Paraguay: locality unknown (USNM105588).

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 RoadAtenquique (TTU 8700, 8701), 2.6 mi SW Atenquique, CuevaQuemada (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 (USNM391094, 391096, 391097). Paraguay: Department Canindeyu,Reserva Natural del Bosque M’Baracayu, 0.9 km E Head quar -ters (TTU 94040).

A. obscurus (n = 5) ― Bolivia: El Beni, Rio Cureraba, BeniReserve (USNM 564325), Rio Mattos, Beni Reserve nearRancho Totaizal (USNM 564326); Santa Cruz, Parque NacionalKempff Mercado (USNM 584490, 584491). French Guiana:Cayenne, Sinnamary (AMNH 266288).

A. planirostris (n = 10) ― Argentina: Jujuy, Yuto (AMNH180303). Ecuador: Napo, Loreto, San Jose Nuevo (AMNH67920). 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 (USNM565533). St. Vincent and the Grenadines: Carriacou (CM63370).

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: Guer -rero, 24.1 mi N Rio La Union Hwy 200 (TTU 35544, 35546);Nayarit, Rio Canas (TTU 33473).

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