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Journal of Mammalogy 90(6):1487-1494. 2009
doi: 10.1644/08-MAMM-A-372R1.1
Taxonomic Status of Artibeus anthonyi (Chiroptera: Phyllostomidae), a Fossil Bat from Cuba
Fernando Balseiroa, Carlos A. Mancinab, and JoséAntonio Guerrero*c
aDivisión de Colecciones Zoológicas, Instituto de Ecología y Sistemática, Ministerio de Ciencia, Tecnología y Medio Ambiente, Carretera de Varona km 3 1/2, Capdevila, Boyeros, Ciudad de La Habana, Cuba
bDivisión de Zoología, Instituto de Ecología y Sistemática, CITMA, Carretera de Varona, km 3 1/2, Capdevila, Boyeros, Ciudad de La Habana, Cuba
cLaboratorio de Sistemática y Morfología, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Avenida Universidad 1001, C.P. 62210 Cuernavaca, Morelos, México
*Correspondent: aguerrero@uaem.mx
Associate Editor was Carey Krajewski.
Abstract
The subgenus Artibeus includes 8 species of frugivorous bats of widespread neotropical distribution. The only fossil species, Artibeus anthonyi, was described from deposits of the Cuban Quaternary, and its taxonomic status has been debated in the literature. Based on exceptionally well-preserved new fossil material, an emended diagnosis and a detailed description of the cranium of A. anthonyi are presented. In addition, we used multivariate analyses to explore the morphometric differentiation between A. anthonyi and the extant species of the subgenus Artibeus. A. anthonyi shows the greatest morphological divergence compared with extant Artibeus species.
Received: December 3, 2008; Accepted: April 6, 2009
Keywords: Artibeus anthonyi, Cuba, fossil bat, morphometrics, taxonomy
The taxonomy of the neotropical bat genus Artibeus has been controversial within the Stenodermatinae (e.g., Guerrero et al. 2008; Handley 1987; Lim 1997; Marques-Aguiar 1994). Specifically, the debate regarding species definitions and distribution of the so-called “Artibeus jamaicensis complex” has lasted for a century (Larsen et al. 2007). Disagreement among authors has been mainly a consequence of different interpretations of morphological variation and geographical distribution of species. The most recent taxonomic arrangement of Artibeus recognized 3 subgenera: Koopmania, Artibeus, and Dermanura, with the nominal subgenus including 8 extant species (Simmons 2005).
To date, the only known extinct species of the subgenus Artibeus is A. anthonyi from the Quaternary of Cuba. Anthony (1919) 1st noted that fossil material he obtained in a cave from eastern Cuba was “quite noticeably larger” than A. jamaicensis (the Cuban extant form). Because of the fragmentary nature of the fossils, he was unable to describe its morphology and treated it as “Artibeus jamaicensis in broad sense.” Woloszyn and Silva (1977) subsequently examined additional fossil remains referable to Anthony's large Artibeus and, after comparisons with specimens of A. jamaicensis parvipes, these authors described the Cuban fossils as A. anthonyi. However, they did not provide detailed comparisons with other subspecies of A. jamaicensis or other species of the subgenus Artibeus.
There are 3 extant forms of Artibeus in the Caribbean Basin. One is A. jamaicensis, which is distributed in Middle America, western Colombia, and the Greater and Lesser Antilles at least as far south as St. Vincent. A 2nd species is A. planirostris, which is distributed in South America east of the Andes, and occurs in the southern Lesser Antilles northward to St. Lucia. A 3rd species is A. schwartzi, which is genetically distinct from A. jamaicensis and A. planirostris and is restricted mainly to St. Vincent (Larsen et al. 2007). Based on apparent morphological similarities, Phillips et al. (1989) speculated that A. schwartzi is a relictual population of A. anthonyi, whereas Pumo et al. (1996) hypothesized that A. anthonyi represented an early Antillean arrival of A. planirostris. Neither of these studies directly compared extant species with specimens of the fossil species.
Exceptionally well-preserved new fossil material that is referable to A. anthonyi was recently recovered from a cave deposit in western Cuba. Based on this material, we reexamined and complemented the original description of A. anthonyi, and improved its differential diagnosis relative to other species of subgenus Artibeus. In addition, we used univariate and multivariate analyses to comprehensively describe patterns of morphometric variation and differentiation between A. anthonyi and extant species.
Materials and Methods
Specimens examined
Forty-nine fossil specimens referable to A. anthonyi were included in this study. This material included complete, nearly complete, and fragmentary fossil skulls. To date, the best-preserved specimens of A. anthonyi (Fig. 1) have been found in Cueva GEDA, which opens in the limestone hill named Sierra La Guasasa (22°39′14.8″N, 83°42′50.3″W), Viñales, Pinar del Rio Province; the main entrance is 70 m above the level of the surrounding valley. The cave has 2 gallery levels. Most of the skeletal remains were found in the floor surface of the 2nd gallery level, not buried by sediments. All fossils were extremely fragile and chalky in appearance. Some specimens were found in anatomical position, similar to the specimens reported by Czaplewski et al. (2003) from Cebada Cave in Belize. At present, a small population of A. j. parvipes inhabits the main entrance of Cueva GEDA. Mancina and García (2005) reported the extinct mammal fauna (including bats) occurring in this fossil deposit.
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Fig. 1 Lateral, ventral, and dorsal views of skull and mandible of a specimen (uncataloged) of Artibeus anthonyi collected in Cueva GEDA.
In the present study, the type series also was reexamined and all the fossil material was compared with the type series. Additional skulls of A. anthonyi were examined from 2 other localities: Cueva El Abrón, Pinar del Río Province (described by Suárez and Díaz-Franco 2003), and Cueva Grande de Judas, Sancti Spiritus Province (the fossil material was provided by A. Hernández, Museo de Historia Natural de la Provincia de Sancti Spiritus). Seventy-five skulls of fossil and recent A. j. parvipes (from 18 localities throughout the country) and 494 skulls of 7 other species of the subgenus Artibeus also were included in this study (see appendix in Guerrero et al. [2003] for information on geographic sources of specimens, and museums where they are stored).
Morphometric analysis
Two approaches were taken for morphometric analysis. The 1st approach involved morphometric comparisons of specimens of A. anthonyi (including the type series) with specimens of A. j. parvipes, the only extant member of the subgenus Artibeus inhabiting Cuba (Genoways et al. 1998; Silva 1979). For this analysis, 14 cranial measurements were taken using calipers and an ocular micrometer (precision ± 0.1 mm): greatest length of skull breadth at mastoids, braincase breadth, zygomatic breadth, postorbital breadth, canine breadth, maxillary breadth, maxillary toothrow length, dentary length, and dentary thickness beneath m1 (following Freeman [1981] and Kalko and Handley [1994]), antorbital width (following Silva [1979]), length of the rostrum (= length from anteriormost point of the lacrimal ridge to anteriormost point of the premaxillae), supraorbital ridge–premaxillary length, and width of 1st upper molar (= greatest labial–lingual width of M1); the distances between teeth in edentulous crania were inferred from external borders of the alveoli. We used a paired t-test to evaluate statistical significance of differences between group means for each character. Specimens used in these comparisons are listed in Appendix I.
The 2nd group of analyses was conducted to assess craniometric comparisons of A. anthonyi with extant species of the subgenus Artibeus (A. amplus, A. fimbriatus, A. fraterculus, A. hirsutus, A. jamaicensis, A. lituratus, A. obscurus, and A. planirostris) by means of multivariate analysis. For these analyses, we evaluated morphometric variation in 9 cranial characters reported by Guerrero et al. (2003) as follows: greatest length of skull, greatest mastoid breadth, braincase width, width of postorbital constriction, length of rostrum, condylobasal length, width of rostrum across M2s, width of M1, and width of posterior border of the hard palate. These characters were selected because the same measurements could be assessed on fossil specimens. Complete and nearly complete skulls of A. anthonyi (n = 8) were then digitized using a Sony Cyber-shot DSC-S750 camera (Sony Electronics Inc., Tokyo, Japan), and cranial dimensions were recorded by using Image Pro Plus software (Media Cybernetics 1994), as described by Guerrero et al. (2003).
A discriminant function analysis was performed to examine multivariate differentiation among species and to identify which characters were more useful in detecting these differences. Squared Mahalanobis distances (D2) were calculated from pairwise comparisons as a measure of morphometric divergence among taxa examined, and then a dendogram was constructed employing the unweighted pairgroup method using arithmetic averages. All statistical analyses were performed using Statistica 6 (StatSoft 1998).
Results
Emended differential diagnosis
Artibeus anthonyi is a recognizable and morphologically distinct species included in the subgenus Artibeus sensu Simmons (2005) with the following combination of characters, emended from the original diagnosis by Woloszyn and Silva (1977): skull, mandibles, and dentition large and massive, larger than most other species of Artibeus; premaxillary bone does not project anteriorly between upper canines; M3 always absent; rostral shield weakly developed with convergent margins; postorbital processes not developed; postorbital constriction broad; m1 with relatively poorly developed hypocone.
By comparison, other species of the subgenus Artibeus differ from A. anthonyi as follows: all populations of A. jamaicensis from the Caribbean with less massive skull, mandibles, and dentition (Genoways et al. 1998, 2007; Pedersen et al. 2007); premaxillary bone usually projected anteriorly between upper canines in A. jamaicensis (sensu Larsen et al. 2007). The M3 is present in A. planirostris and A. amplus (Genoways et al. 1998; Guerrero et al. 2008; Hollis 2005). Rostral shield is well developed with nearly parallel lateral margins in A. amplus (Lim and Wilson 1993). In A. lituratus the rostral shield is well developed, with remarkable preorbital and postorbital processes, and the postorbital constriction is narrower (Marques-Aguiar 1994). Cranial measurements are markedly smaller (see Guerrero et al. 2003) and the mesopterigoid fossa is constricted posteriorly on the basicranium in A. hirsutus and A. inopinatus (Marques-Aguiar 1994). A well-developed hypocone is present in the M1 of A. fraterculus (Marques-Aguiar 1994). In addition, the postorbital constriction is immediately behind the postorbital processes in A. fraterculus. A. fimbriatus presents larger skulls (mean greatest length of skull, 31.1 mm—Handley 1990). We were unable to examine specimens referable to A. schwartzi (a species recently recognized by Larsen et al. [2007]), but several characters described by Genoways et al. (1998) and Jones (1978) provide a basis for morphometric comparisons. A. schwartzi is characterized by a larger skull (greatest length of skull, 30.1–31.8 mm; zygomatic breadth, 18.6–20.1 mm; maxillary toothrow length, 10.4–11.4 mm; breadth at mastoids, 13.5–14.7 mm) compared to A. anthonyi (greatest length of skull, 28.6–29.8 mm; zygomatic breadth, 17.3–18.0 mm; maxillary toothrow length, 9.8–10.9 mm; breadth at mastoids, 12.6–14.0 mm).
Redescription of Artibeus anthonyi Woloszyn and Silva, 1977
The skull of A. anthonyi is massive with the braincase domed in lateral view (Fig. 1). The sagittal ridge is marked in the anterior half of the braincase but only moderately developed in the posterior half. Premaxillary bone slightly or not projected between canines. Incisive foramina medium sized, extending past posterior margin of canines between level of C and P1. Outline of external narial opening trapezoidal to pentagonal with rounded angles. Posterior (dorsal) border of nasal foramen slightly wavy (medial notch present) or completely straight. Rostral shield absent. Anterior vertex of the orbit broadly rounded. Supraorbital ridges weakly to moderately developed. Postorbital ridges obsolete. Preorbital process not well developed. Postorbital process absent to moderately developed. Rostrum depressed at the rostral angle. Postorbital constriction broad (in the sense of Marques-Aguiar 1994) and well behind postorbital process. Zygomatic arches diverge markedly posteriorly, their general morphology as described by Woloszyn and Silva (1977). Hard palate broad with small backward-directed projections sometimes present on the posterior border. Postpalatal region as broad as long and with small, lateral, pointed projections present or not. Mesopterygoid fossa U-shaped or sometimes with squared vertex, never V-shaped, and with parallel or subparallel lateral borders. Maxillary toothrows converge anteriorly. Basisphenoid pits shallow to moderately developed. Paraoccipital processes present but scarcely developed. Mandible is essentially as described by Woloszyn and Silva (1977). Ventral border of horizontal ramus slightly convex (Fig. 1). Coronoid process is nearly as wide at the base as high. Internal ridge of coronoid moderately developed especially at the midpoint. Angle of the ascending ramus ranges from right to nearly obtuse. Internal ridge of angular process marked and not pointed. Distal border of coronoid process almost completely straight and forming an obtuse angle with horizontal plane. Border between angular and articular process straight or slightly curved. Dental formula is i 2/2, c 1/1, p 2/2, m 2/3, total 30. Inner upper incisors bifid, internal lobe more developed than external, cutting edge slightly oblique, laterally in contact in the lower halves and divergent in the upper halves. Outer upper incisors are rectangular and noticeably oblique with cutting edge straight for nearly all of its length, but a small distal cusp is present. Lower incisors equal in size and in contact with each other. Upper canines are large and lack basal cusps. Lateral surfaces bear a longitudinal groove. The cingulum thickens at the meeting points with P1 and outer upper incisors, with a small projection at the base of the lingual face. Lower canines smaller than uppers, with no conspicuous basal cusp. Crown of P1 rectangular and oblique in labial view. It presents a main cusp mesially and a less-developed secondary cusp distally. Internal surface of P1 distolingually oriented and flat or slightly concave, cingulum poorly developed in this surface. The p1 is rhomboidal in labial view with a main cusp in the midpoint of the mesiodistal axis, and a blunt distal secondary cusp. Crown of p1 longer than high. There is scarce development of the cingulum lingually. Lingual surface is triangular and flat. P2 is triangular labially, and is higher than long, with a medial main cusp and poorly developed distal cusp. P2 cingulum expanded lingually, surrounding a concave base and bearing 1 conspicuous mesial basal cusp. p2 with a prominent mesial cusp, nearly as high as lower canine cusp. A secondary blunt distal cusp also is present. Lingual cingulum poorly developed not bearing basal cusp and slightly directed distally. Lingual surface constrained by the mesial descendent cingulum. M1 is longer at lingual than at labial surface, and is broader than any other tooth. Paracone and metacone lobes attached to the labial margin, the paracone being the tallest. The protocone occurs mesially and the hypocone is distally displaced. Both cusps nearly the same height and included in the cingulum. A concave and broad grinding surface is present between lingual and labial cusps. The m1 is longer than broad, with 2 labial and 2 lingual cusps nearly equal in size. Labial and lingual margins are parallel in their distal halves but acutely convergent in their mesial halves. There is a broad and concave grinding surface between labial and lingual cusps. M2 is trapezoidal in occlusal outline. A prominent paracone is present mesially in the labial margin. Metacone and metaconule are small but distinct lobes, both distally displaced because of the posterior convergence of the labial and lingual margins of the tooth. Two small lingual cusps also are present. The m2 is as broad as long, with straight mesial margin and distal convergence between labial and lingual margins. The 2 lingual cusps and single labial cusp are set apart by a broad grinding surface as in the m1. M3 is always absent. The m3 is peglike and without cusps, even smaller than lower incisors.
Morphometric comparisons
The mean and range of cranial measurements of A. anthonyi, as well as the results of a t-test comparing that sample with individuals of A. j. parvipes from Cuba, are presented in Table 1. Because no geographic variation within samples of both A. anthonyi and A. j. parvipes was detected in preliminary analysis (results not showed), specimens of all localities were pooled for further comparisons. Individuals of A. anthonyi were significantly larger than those of A. j. parvipes in all of the cranial measurements at the P < 0.01 level. In fact, the range of measurements of the 2 taxa only overlapped in 6 of the 14 measurements. Therefore, we considered the skull of the extinct A. anthonyi as morphometrically distinct from the recent Cuban form of A. jamaicensis.
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Table 1 Cranial measurements (mm) of Artibeus anthonyi and A. jamaicensis from Cuba, mean ± 1 SD, range in parentheses, and sample size (n). Sample of A. jamaicensis includes recent, subfossil, and fossil specimens. The type series of A. anthonyi was combined with all new available material for comparisons. All measurements showed significant differences (P < 0.01) among species according to t-tests.
Morphometric differentiation within the subgenus Artibeus
Differentiation among species was assessed by discriminant analysis. Canonical axes 1, 2, and 3, derived from the 9 cranial variables, accounted for 57.2%, 21.2%, and 16.4% of the interspecific variation, respectively (Table 2). A plot of canonical axes 1 and 2 (Fig. 2A) showed a poor craniometrical differentiation among most species, with A. anthonyi occupying an intermediate position in overall size among the large species of Artibeus. However, when canonical axes 1 and 3 were plotted (Fig. 2B), we observed the separation of A. anthonyi along the y axis. This 3rd canonical variate had a high negative correlation with the variables width of the rostrum across the m2s, and width of the postorbital constriction (Table 2), indicating the lowest values of both cranial variables toward the top of the plot.
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Fig. 2 Plots of scores of A) canonical variates 1 versus 2, and B) canonical variates 1 versus 3 obtained from discriminant function analysis of 9 cranial variables from 9 species of the subgenus Artibeus.
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Table 2 Correlations between canonical variates (CVs) and 9 cranial variables selected for comparisons of recent species of the genus Artibeus and the extinct Artibeus anthonyi.
Unweighted pairgroup method using arithmetic averages clustering showed that A. anthonyi is well distinguished from the 8 other species of Artibeus (Fig. 3). The Cuban fossil showed the greatest values of cranial divergence in terms of Mahalanobis distance with respect to other Artibeus species (Table 3). The greatest morphological divergence occurred between A. anthonyi and A. planirostris (D2 = 47.6), followed by that between A. anthonyi and A. obscurus (D2 = 44.8). A. anthonyi showed the least divergence from A. amplus (D2 = 19.3).
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Fig. 3 Dendrogram constructed employing the unweighted pairgroup method using arithmetic averages based on Mahalanobis distances for 9 species of the subgenus Artibeus.
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Table 3 Morphometric divergence between species of Artibeus examined as indicated by Mahalanobis distances (D2).
Discussion
Based on morphological similarities, Phillips et al. (1989) speculated that A. schwartzi from St. Vincent is a relictual population of A. anthonyi. Pumo et al. (1996), noting the supposed morphological similitude between A. anthonyi and A. planirostris, hypothesized that A. anthonyi represents an early arrival to the Antilles of A. planirostris, and that it lost its taxonomic identity through hybridization with A. jamaicensis. These hypotheses do not gain further support when considered in light of our results. Among all species of the subgenus Artibeus we found the 2nd greatest cranial divergence between A. anthonyi and A. planirostris (exceeded only by the difference between A. anthonyi and A. obscurus). Although A. anthonyi exhibits similarity to A. planirostris in some craniometrical characters, these species (and maybe A. schwartzi) differ in their cranial appearance. Likewise, we found little or no morphometric overlap between A. anthonyi and samples of the extant A. jamaicensis from Cuba. Other elements, such as the doubtful coexistence of A. anthonyi and A. jamaicensis in the Cuban Holocene (see below) and the lack of large Artibeus fossils from Cuba and other islands north of St. Vincent (Morgan 2001), do not support the hybridization hypotheses. On the other hand, Larsen et al. (2007) included A. j. trinitatis in the phylogenetic species A. planirostris. Guerrero et al. (2004) found high molecular divergence between triomylus and jamaicensis and suggested full species rank for triomylus. These molecular studies indirectly support the presence–absence of M3 as a diagnostic character for the separation between Antillean and continental species.
That A. anthonyi shows a high cranial divergence from extant mainland Artibeus and that it was geographically restricted to Cuba suggest that it could be an ancient lineage within Artibeus. To date, hypotheses about the South American origin of A. anthonyi have prevailed (Phillips et al. 1989; Pumo et al. 1996; Woloszyn and Silva 1977), but dispersal routes from Mexico or Central America, or both, to Cuba also have been proposed for stenodermatine bats (Koopman 1989). These hypotheses can be tested by inferring phylogenetic relationship among extant and fossil taxa.
Radiocarbon dates made directly on fossil material of A. anthonyi are unavailable today. However, samples of bones from 2 fossil deposits that include remains of A. anthonyi formed by the accumulation of barn owl (Tyto alba) pellets have been dated. One of these deposits gave ages ranging from 20,050 to 21,474 years ago (Suárez and Díaz-Franco 2003). The 2nd deposit yielded an age of 7,864 ± 96 years ago (Jiménez et al. 2005); however, because of the nature of this deposit the date could not reliably predict the age of the remains of A. anthonyi at the site.
Fossil specimens of A. anthonyi are commonly found in Quaternary cave deposits throughout Cuba, demonstrating that this species had a widespread distribution on the island. The extinction of A. anthonyi may have been caused by climatic changes that occurred in the late Pleistocene or early Holocene (see Curtis et al. 2001). Similar to other extinct Cuban stenodermatines (i.e., Phyllops vetus, P. silvai, and Cubanycteris silvai), a change to a drier climate in the Holocene could have caused changes in the distribution and abundance of resources such as fruits, strongly impacting these tree-dwelling bats. In recent time, populations of arboricolous bats on West Indian islands have been reduced after these islands were impacted by hurricanes (Gannon and Willig 1994; Pedersen et al. 1996). No evidence exists about the effect of competition by A. jamaicensis on the decline or extinction of populations of A. anthonyi as suggested by Woloszyn and Silva (1977). Strong evidence, such as molecular data, and the lack of specimens of A. jamaicensis in fossil deposits from some islands, suggests that A. jamaicensis recently invaded the Antilles across the Yucatan Channel into Cuba or Jamaica during the late Pleistocene, after the West Indies acquired their present form (Genoways et al. 2005; Larsen et al. 2007; Morgan 1989, 2001). Probably, at the time that A. jamaicensis reached Cuba, populations of A. anthonyi were declining or extinct. To date, there are no data supporting the coexistence of both species of Artibeus on Cuba. Anthony (1919) found some specimens of the “large form” (A. anthonyi) encrusted with lime, whereas the remaining Artibeus in the deposit “were in a loose earthy formation and had not become cemented.” Likewise, in other deposits where A. anthonyi has been recorded, no remains of A. jamaicensis were found (Jimenez et al. 2005; Suárez and Díaz-Franco 2003). In Cueva GEDA, preliminary observations on the fluorine content in bones of A. anthonyi and A. jamaicensis suggest that the former is older than the latter. In this deposit, specimens of A. anthonyi are more abundant than those of A. jamaicensis, whereas the opposite has been found in other deposits containing A. anthonyi (Woloszyn and Silva 1977). Unlike other Cuban deposits bearing the extinct Artibeus, Cueva GEDA certainly represents equivalence between the biocenosis and taphocenosis. Therefore, further taphonomic studies of the site should clarify questions related to the colonization and extinction of this species. On the other hand, DNA sequence from fossil material of A. anthonyi could help explain the origin and the phylogenetic relationships of the genus Artibeus throughout the Caribbean region.
Resumen
El subgénero Artibeus incluye 8 especies de murciélagos frugívoros de amplia distribución neotropical. La única especie fósil, Artibeus anthonyi, fue descrita de los depósitos Cuaternarios de Cuba, y su estado taxonómico ha sido controversial en la literatura. Con base en nuevo material fósil excepcionalmente bien preservado, una diagnosis enmendada de la especie y la descripción detallada del cráneo del murciélago fósil Artibeus son presentadas. A través de análisis multivariados exploramos la diferenciación morfométrica de A. anthonyi y las otras especies del subgénero Artibeus. El fósil cubano de Artibeus muestra la mayor divergencia morfológica entre los Artibeus existentes.
Acknowledgments
This project was supported by Zoological Collection Program of Instituto de Ecología y Systemática. We thank M. Condis, H. Farfán, L. D. Torres, C. Aldana, R. Rivera, and members of GEDA Group (Sociedad Espeleológica de Cuba) for direct assistance in the fieldwork. A. Hernández, W. Suárez, and G. Silva kindly provided fossil material for comparisons. Comments from 2 reviewers greatly improved the clarity of the manuscript.
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24. Morgan, G. S. 1989. Fossil chiroptera and rodentia from the Bahamas, and the historical biogeography of the Bahamian mammal fauna. 685–740. in Biogeography of the West Indies: past, present, and future. Woods, C. A. Sandhill Crane Press. Gainesville, Florida.
25. Morgan, G. S. 2001. Patterns of extinction in West Indian bats. 369–407. in Biogeography of the West Indies: patterns and perspectives. Woods, C. A. and F. E. Sergile. 2nd ed. CRC Press. Boca Raton, Florida.
26. Pedersen, S. C., H. H. Genoways, and P. W. Freeman. 1996. Notes on bats from Montserrat (Lesser Antilles) with comments concerning the effects of Hurricane Hugo. Caribbean Journal of Science 32:206–213.
27. Pedersen, S. C., P. A. Larsen, H. H. Genoways, M. N. Morton, K. C. Lindsay, and J. Cindric. 2007. Bats of Barbuda, northern Lesser Antilles. Occasional Papers, Museum of the Texas Tech University 271:1–19.
28. Phillips, C. J., D. E. Pumo, H. H. Genoways, and P. E. Ray. 1989. Caribbean island zoogeography: a new approach using mitochondrial DNA to study neotropical bats. 661–684. in Biogeography of the West Indies: past, present, and future. Woods, C. A. Sandhill Crane Press. Gainesville, Florida.
29. Pumo, D. E., I. Kim, J. Remsen, C. J. Phillips, and H. H. Genoways. 1996. Molecular systematics of the fruit bat, Artibeus jamaicensis: origin of an unusual island population. Journal of Mammalogy 77:491–503. CrossRef, CSA
30. Silva, G. 1979. Los murciélagos de Cuba. Editorial Academia. La Habana, Cuba.
31. Simmons, N. B. 2005. Order Chiroptera. 312–529. in Mammal species of the world: a taxonomic and geographic reference. Wilson, D. E. and D. M. Reeder. 3rd ed. Johns Hopkins University Press. Baltimore, Maryland.
32. StatSoft 1998. Statistica 6.0 for Windows. StatSoft. Tulsa, Oklahoma.
33. Suárez, W. and S. DÍaz-Franco. 2003. A new fossil bat (Chiroptera: Phyllostomidae) from a Quaternary cave deposit in Cuba. Caribbean Journal of Science 39:371–377.
34. Woloszyn, B. W. and G. Silva. 1977. Nueva especie fósil de Artibeus (Mammalia: Chiroptera) de Cuba, y tipificación preliminar de los depósitos fosilíferos cubanos contentivos de mamíferos terrestres. Poeyana 161:1–17.
Appendix I
Specimens examined
Gazetteer of specimens and collecting localities of Artibeus jamaicensis parvipes and A. anthonyi. Provinces are listed in uppercase letters followed by specific localities, and latitude and longitude in paretheses. Specimens are deposited in the following collections: Zoological Collection of the Instituto de Ecología y Sistematica, Ciudad Habana (CZACC); past Collection of Instituto de Zoología, Academia de Ciencias de Cuba (IZ); and Paleontological Collection of Museo Nacional de Historia Natural de Cuba (MNHNCu).
Artibeus jamaicensis parvipes (fresh material)
PINAR DEL RÍO: Cueva del Indio, San Diego de los Baños (22°56′N, 82°57′W), CZACC 1. 2224, 1. 2228, 1. 2232. CIUDAD DE LA HABANA: El Laguito, Playa (23°05′N, 82°28′W), CZACC 1. 2221, 1. 2222; Quinta de los Molinos, Cerro [past Botanical Garden] (23°06′N, 82°23′W), CZACC 1. 2245. PROVINCIA HABANA: Cueva Cayamas, Isla de la Juventud (21°49′N, 82°42′W), CZACC 1. 2196, 1. 2201, 1. 2205, 1. 2208. MATANZAS: Cueva de Los Murciélagos, Bacunayagua (23°05′N, 81°20′W), CZACC 1. 2294; Cueva de Los Murciélagos, Jagüey Grande (22°30′N, 81°09′W), CZACC 1. 2189, 1. 2192; Cueva de Santa Catalina, Camarioca (23°05′N, 81°24′W), 1. 2292. CIENFUEGOS: Jardín Botánico, Soledad (22°07′N, 80°20′W), CZACC 1. 2161, 1. 2162, 1. 2275, 1. 2276, 1. 2278; small cave beneath the road that passes over the Yaguanabo River (21°51′N, 80°13′W), CZACC 1. 2179, 1. 2180, 1. 2182, 1. 2184. SANCTI SPIRITUS: Cueva de Los Murciélgos, Sierra de Esperanza (22°01′N, 79°27′W), CZACC 1. 2297. CAMAGÜEY: Cueva Ñico López, Esmeralda (21°51′N, 78°06′W), CZACC 1. 2172; Cueva Maraguán, Camagüey (21°21′N, 77°45′W), CZACC 1. 2256. HOLGUÍN: Cueva Estrada, El Almirante (20°56′N, 76°11′W), CZACC 1. 2163, 1. 2165. SANTIAGO DE CUBA: Embalse Chalons, Santiago de Cuba (20°04′N, 75°49′W), CZACC 1. 2274; Cueva de la Cantera, Siboney (19°58′N, 75°43′W), CZACC 1. 2212, 1. 2216, 1. 2218, 1. 2268, 1. 2269.
Artibeus jamaicensis parvipes (fossil or subfossil material)
PINAR DEL RÍO: Cueva GEDA, Viñales (22°39′N, 83°42′W), [skulls] CZACC 26. 1941, 26. 1942. CIUDAD HABANA: Cueva de la Santa, Bacuranao (23°11′N, 82°12′W), [skull] CZACC 26. 1943. SANCTI SPIRITUS: Cueva Grande, Punta Judas (22°23′N, 79°00′W), [skulls] CZACC 26. 1919, 26. 1920.
Artibeus anthonyi
PINAR DEL RÍO: Cueva GEDA, Viñales (22°39′N, 83°42′W), [skull + mandibles] CZACC 26. 1933, 26. 1934, 26. 1937, 26. 1938; [skull] CZACC 26. 1935, 26. 1936, 26. 1939, 26. 1940; Cueva El Abrón, Los Palacios (22°40′N, 83°28′W), [skulls] MNHNCu 76. 4652–76. 4665. PROVINCIA HABANA: Cueva Paredones, Ceiba del Agua, Caimito (22°52′N, 82°38′W), [skull] CZACC 26. 1900. SANCTI SPIRITUS: quarry in a limestone hill near Moza, 5 km NE from Sancti Spiritus (21°57′N, 79°25′W), [skull] CZACC 26. 1891 [IZ-344.5, paratype]; Cueva del Centenario de Lenin, Punta Judas (22°21′N, 79°00′W), [skulls] CZACC 26. 1888 [IZ-344.2, holotype], 26. 1889 [IZ-344.3, paratype], 26. 1890 [IZ-344.4, paratype]; Cueva Grande, Punta Judas (22°21′N, 79°00′W), [skulls] CZACC 26. 1911–26. 1918, 26. 1921–26. 1925; [mandibles] CZACC 26. 1893 [IZ-344.6], 26. 1926–26. 1929.
www.bioone.org/doi/full/10.1644/08-MAMM-A-372R1.1?prevSearch=%255Bfulltext%253A%2Banthony%2Bquaternary%255D%2BAND%2B%255Bpublisher%253A%2Bbioone%255D&searchHistoryKey=
doi: 10.1644/08-MAMM-A-372R1.1
Taxonomic Status of Artibeus anthonyi (Chiroptera: Phyllostomidae), a Fossil Bat from Cuba
Fernando Balseiroa, Carlos A. Mancinab, and JoséAntonio Guerrero*c
aDivisión de Colecciones Zoológicas, Instituto de Ecología y Sistemática, Ministerio de Ciencia, Tecnología y Medio Ambiente, Carretera de Varona km 3 1/2, Capdevila, Boyeros, Ciudad de La Habana, Cuba
bDivisión de Zoología, Instituto de Ecología y Sistemática, CITMA, Carretera de Varona, km 3 1/2, Capdevila, Boyeros, Ciudad de La Habana, Cuba
cLaboratorio de Sistemática y Morfología, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Avenida Universidad 1001, C.P. 62210 Cuernavaca, Morelos, México
*Correspondent: aguerrero@uaem.mx
Associate Editor was Carey Krajewski.
Abstract
The subgenus Artibeus includes 8 species of frugivorous bats of widespread neotropical distribution. The only fossil species, Artibeus anthonyi, was described from deposits of the Cuban Quaternary, and its taxonomic status has been debated in the literature. Based on exceptionally well-preserved new fossil material, an emended diagnosis and a detailed description of the cranium of A. anthonyi are presented. In addition, we used multivariate analyses to explore the morphometric differentiation between A. anthonyi and the extant species of the subgenus Artibeus. A. anthonyi shows the greatest morphological divergence compared with extant Artibeus species.
Received: December 3, 2008; Accepted: April 6, 2009
Keywords: Artibeus anthonyi, Cuba, fossil bat, morphometrics, taxonomy
The taxonomy of the neotropical bat genus Artibeus has been controversial within the Stenodermatinae (e.g., Guerrero et al. 2008; Handley 1987; Lim 1997; Marques-Aguiar 1994). Specifically, the debate regarding species definitions and distribution of the so-called “Artibeus jamaicensis complex” has lasted for a century (Larsen et al. 2007). Disagreement among authors has been mainly a consequence of different interpretations of morphological variation and geographical distribution of species. The most recent taxonomic arrangement of Artibeus recognized 3 subgenera: Koopmania, Artibeus, and Dermanura, with the nominal subgenus including 8 extant species (Simmons 2005).
To date, the only known extinct species of the subgenus Artibeus is A. anthonyi from the Quaternary of Cuba. Anthony (1919) 1st noted that fossil material he obtained in a cave from eastern Cuba was “quite noticeably larger” than A. jamaicensis (the Cuban extant form). Because of the fragmentary nature of the fossils, he was unable to describe its morphology and treated it as “Artibeus jamaicensis in broad sense.” Woloszyn and Silva (1977) subsequently examined additional fossil remains referable to Anthony's large Artibeus and, after comparisons with specimens of A. jamaicensis parvipes, these authors described the Cuban fossils as A. anthonyi. However, they did not provide detailed comparisons with other subspecies of A. jamaicensis or other species of the subgenus Artibeus.
There are 3 extant forms of Artibeus in the Caribbean Basin. One is A. jamaicensis, which is distributed in Middle America, western Colombia, and the Greater and Lesser Antilles at least as far south as St. Vincent. A 2nd species is A. planirostris, which is distributed in South America east of the Andes, and occurs in the southern Lesser Antilles northward to St. Lucia. A 3rd species is A. schwartzi, which is genetically distinct from A. jamaicensis and A. planirostris and is restricted mainly to St. Vincent (Larsen et al. 2007). Based on apparent morphological similarities, Phillips et al. (1989) speculated that A. schwartzi is a relictual population of A. anthonyi, whereas Pumo et al. (1996) hypothesized that A. anthonyi represented an early Antillean arrival of A. planirostris. Neither of these studies directly compared extant species with specimens of the fossil species.
Exceptionally well-preserved new fossil material that is referable to A. anthonyi was recently recovered from a cave deposit in western Cuba. Based on this material, we reexamined and complemented the original description of A. anthonyi, and improved its differential diagnosis relative to other species of subgenus Artibeus. In addition, we used univariate and multivariate analyses to comprehensively describe patterns of morphometric variation and differentiation between A. anthonyi and extant species.
Materials and Methods
Specimens examined
Forty-nine fossil specimens referable to A. anthonyi were included in this study. This material included complete, nearly complete, and fragmentary fossil skulls. To date, the best-preserved specimens of A. anthonyi (Fig. 1) have been found in Cueva GEDA, which opens in the limestone hill named Sierra La Guasasa (22°39′14.8″N, 83°42′50.3″W), Viñales, Pinar del Rio Province; the main entrance is 70 m above the level of the surrounding valley. The cave has 2 gallery levels. Most of the skeletal remains were found in the floor surface of the 2nd gallery level, not buried by sediments. All fossils were extremely fragile and chalky in appearance. Some specimens were found in anatomical position, similar to the specimens reported by Czaplewski et al. (2003) from Cebada Cave in Belize. At present, a small population of A. j. parvipes inhabits the main entrance of Cueva GEDA. Mancina and García (2005) reported the extinct mammal fauna (including bats) occurring in this fossil deposit.
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Fig. 1 Lateral, ventral, and dorsal views of skull and mandible of a specimen (uncataloged) of Artibeus anthonyi collected in Cueva GEDA.
In the present study, the type series also was reexamined and all the fossil material was compared with the type series. Additional skulls of A. anthonyi were examined from 2 other localities: Cueva El Abrón, Pinar del Río Province (described by Suárez and Díaz-Franco 2003), and Cueva Grande de Judas, Sancti Spiritus Province (the fossil material was provided by A. Hernández, Museo de Historia Natural de la Provincia de Sancti Spiritus). Seventy-five skulls of fossil and recent A. j. parvipes (from 18 localities throughout the country) and 494 skulls of 7 other species of the subgenus Artibeus also were included in this study (see appendix in Guerrero et al. [2003] for information on geographic sources of specimens, and museums where they are stored).
Morphometric analysis
Two approaches were taken for morphometric analysis. The 1st approach involved morphometric comparisons of specimens of A. anthonyi (including the type series) with specimens of A. j. parvipes, the only extant member of the subgenus Artibeus inhabiting Cuba (Genoways et al. 1998; Silva 1979). For this analysis, 14 cranial measurements were taken using calipers and an ocular micrometer (precision ± 0.1 mm): greatest length of skull breadth at mastoids, braincase breadth, zygomatic breadth, postorbital breadth, canine breadth, maxillary breadth, maxillary toothrow length, dentary length, and dentary thickness beneath m1 (following Freeman [1981] and Kalko and Handley [1994]), antorbital width (following Silva [1979]), length of the rostrum (= length from anteriormost point of the lacrimal ridge to anteriormost point of the premaxillae), supraorbital ridge–premaxillary length, and width of 1st upper molar (= greatest labial–lingual width of M1); the distances between teeth in edentulous crania were inferred from external borders of the alveoli. We used a paired t-test to evaluate statistical significance of differences between group means for each character. Specimens used in these comparisons are listed in Appendix I.
The 2nd group of analyses was conducted to assess craniometric comparisons of A. anthonyi with extant species of the subgenus Artibeus (A. amplus, A. fimbriatus, A. fraterculus, A. hirsutus, A. jamaicensis, A. lituratus, A. obscurus, and A. planirostris) by means of multivariate analysis. For these analyses, we evaluated morphometric variation in 9 cranial characters reported by Guerrero et al. (2003) as follows: greatest length of skull, greatest mastoid breadth, braincase width, width of postorbital constriction, length of rostrum, condylobasal length, width of rostrum across M2s, width of M1, and width of posterior border of the hard palate. These characters were selected because the same measurements could be assessed on fossil specimens. Complete and nearly complete skulls of A. anthonyi (n = 8) were then digitized using a Sony Cyber-shot DSC-S750 camera (Sony Electronics Inc., Tokyo, Japan), and cranial dimensions were recorded by using Image Pro Plus software (Media Cybernetics 1994), as described by Guerrero et al. (2003).
A discriminant function analysis was performed to examine multivariate differentiation among species and to identify which characters were more useful in detecting these differences. Squared Mahalanobis distances (D2) were calculated from pairwise comparisons as a measure of morphometric divergence among taxa examined, and then a dendogram was constructed employing the unweighted pairgroup method using arithmetic averages. All statistical analyses were performed using Statistica 6 (StatSoft 1998).
Results
Emended differential diagnosis
Artibeus anthonyi is a recognizable and morphologically distinct species included in the subgenus Artibeus sensu Simmons (2005) with the following combination of characters, emended from the original diagnosis by Woloszyn and Silva (1977): skull, mandibles, and dentition large and massive, larger than most other species of Artibeus; premaxillary bone does not project anteriorly between upper canines; M3 always absent; rostral shield weakly developed with convergent margins; postorbital processes not developed; postorbital constriction broad; m1 with relatively poorly developed hypocone.
By comparison, other species of the subgenus Artibeus differ from A. anthonyi as follows: all populations of A. jamaicensis from the Caribbean with less massive skull, mandibles, and dentition (Genoways et al. 1998, 2007; Pedersen et al. 2007); premaxillary bone usually projected anteriorly between upper canines in A. jamaicensis (sensu Larsen et al. 2007). The M3 is present in A. planirostris and A. amplus (Genoways et al. 1998; Guerrero et al. 2008; Hollis 2005). Rostral shield is well developed with nearly parallel lateral margins in A. amplus (Lim and Wilson 1993). In A. lituratus the rostral shield is well developed, with remarkable preorbital and postorbital processes, and the postorbital constriction is narrower (Marques-Aguiar 1994). Cranial measurements are markedly smaller (see Guerrero et al. 2003) and the mesopterigoid fossa is constricted posteriorly on the basicranium in A. hirsutus and A. inopinatus (Marques-Aguiar 1994). A well-developed hypocone is present in the M1 of A. fraterculus (Marques-Aguiar 1994). In addition, the postorbital constriction is immediately behind the postorbital processes in A. fraterculus. A. fimbriatus presents larger skulls (mean greatest length of skull, 31.1 mm—Handley 1990). We were unable to examine specimens referable to A. schwartzi (a species recently recognized by Larsen et al. [2007]), but several characters described by Genoways et al. (1998) and Jones (1978) provide a basis for morphometric comparisons. A. schwartzi is characterized by a larger skull (greatest length of skull, 30.1–31.8 mm; zygomatic breadth, 18.6–20.1 mm; maxillary toothrow length, 10.4–11.4 mm; breadth at mastoids, 13.5–14.7 mm) compared to A. anthonyi (greatest length of skull, 28.6–29.8 mm; zygomatic breadth, 17.3–18.0 mm; maxillary toothrow length, 9.8–10.9 mm; breadth at mastoids, 12.6–14.0 mm).
Redescription of Artibeus anthonyi Woloszyn and Silva, 1977
The skull of A. anthonyi is massive with the braincase domed in lateral view (Fig. 1). The sagittal ridge is marked in the anterior half of the braincase but only moderately developed in the posterior half. Premaxillary bone slightly or not projected between canines. Incisive foramina medium sized, extending past posterior margin of canines between level of C and P1. Outline of external narial opening trapezoidal to pentagonal with rounded angles. Posterior (dorsal) border of nasal foramen slightly wavy (medial notch present) or completely straight. Rostral shield absent. Anterior vertex of the orbit broadly rounded. Supraorbital ridges weakly to moderately developed. Postorbital ridges obsolete. Preorbital process not well developed. Postorbital process absent to moderately developed. Rostrum depressed at the rostral angle. Postorbital constriction broad (in the sense of Marques-Aguiar 1994) and well behind postorbital process. Zygomatic arches diverge markedly posteriorly, their general morphology as described by Woloszyn and Silva (1977). Hard palate broad with small backward-directed projections sometimes present on the posterior border. Postpalatal region as broad as long and with small, lateral, pointed projections present or not. Mesopterygoid fossa U-shaped or sometimes with squared vertex, never V-shaped, and with parallel or subparallel lateral borders. Maxillary toothrows converge anteriorly. Basisphenoid pits shallow to moderately developed. Paraoccipital processes present but scarcely developed. Mandible is essentially as described by Woloszyn and Silva (1977). Ventral border of horizontal ramus slightly convex (Fig. 1). Coronoid process is nearly as wide at the base as high. Internal ridge of coronoid moderately developed especially at the midpoint. Angle of the ascending ramus ranges from right to nearly obtuse. Internal ridge of angular process marked and not pointed. Distal border of coronoid process almost completely straight and forming an obtuse angle with horizontal plane. Border between angular and articular process straight or slightly curved. Dental formula is i 2/2, c 1/1, p 2/2, m 2/3, total 30. Inner upper incisors bifid, internal lobe more developed than external, cutting edge slightly oblique, laterally in contact in the lower halves and divergent in the upper halves. Outer upper incisors are rectangular and noticeably oblique with cutting edge straight for nearly all of its length, but a small distal cusp is present. Lower incisors equal in size and in contact with each other. Upper canines are large and lack basal cusps. Lateral surfaces bear a longitudinal groove. The cingulum thickens at the meeting points with P1 and outer upper incisors, with a small projection at the base of the lingual face. Lower canines smaller than uppers, with no conspicuous basal cusp. Crown of P1 rectangular and oblique in labial view. It presents a main cusp mesially and a less-developed secondary cusp distally. Internal surface of P1 distolingually oriented and flat or slightly concave, cingulum poorly developed in this surface. The p1 is rhomboidal in labial view with a main cusp in the midpoint of the mesiodistal axis, and a blunt distal secondary cusp. Crown of p1 longer than high. There is scarce development of the cingulum lingually. Lingual surface is triangular and flat. P2 is triangular labially, and is higher than long, with a medial main cusp and poorly developed distal cusp. P2 cingulum expanded lingually, surrounding a concave base and bearing 1 conspicuous mesial basal cusp. p2 with a prominent mesial cusp, nearly as high as lower canine cusp. A secondary blunt distal cusp also is present. Lingual cingulum poorly developed not bearing basal cusp and slightly directed distally. Lingual surface constrained by the mesial descendent cingulum. M1 is longer at lingual than at labial surface, and is broader than any other tooth. Paracone and metacone lobes attached to the labial margin, the paracone being the tallest. The protocone occurs mesially and the hypocone is distally displaced. Both cusps nearly the same height and included in the cingulum. A concave and broad grinding surface is present between lingual and labial cusps. The m1 is longer than broad, with 2 labial and 2 lingual cusps nearly equal in size. Labial and lingual margins are parallel in their distal halves but acutely convergent in their mesial halves. There is a broad and concave grinding surface between labial and lingual cusps. M2 is trapezoidal in occlusal outline. A prominent paracone is present mesially in the labial margin. Metacone and metaconule are small but distinct lobes, both distally displaced because of the posterior convergence of the labial and lingual margins of the tooth. Two small lingual cusps also are present. The m2 is as broad as long, with straight mesial margin and distal convergence between labial and lingual margins. The 2 lingual cusps and single labial cusp are set apart by a broad grinding surface as in the m1. M3 is always absent. The m3 is peglike and without cusps, even smaller than lower incisors.
Morphometric comparisons
The mean and range of cranial measurements of A. anthonyi, as well as the results of a t-test comparing that sample with individuals of A. j. parvipes from Cuba, are presented in Table 1. Because no geographic variation within samples of both A. anthonyi and A. j. parvipes was detected in preliminary analysis (results not showed), specimens of all localities were pooled for further comparisons. Individuals of A. anthonyi were significantly larger than those of A. j. parvipes in all of the cranial measurements at the P < 0.01 level. In fact, the range of measurements of the 2 taxa only overlapped in 6 of the 14 measurements. Therefore, we considered the skull of the extinct A. anthonyi as morphometrically distinct from the recent Cuban form of A. jamaicensis.
table
Table 1 Cranial measurements (mm) of Artibeus anthonyi and A. jamaicensis from Cuba, mean ± 1 SD, range in parentheses, and sample size (n). Sample of A. jamaicensis includes recent, subfossil, and fossil specimens. The type series of A. anthonyi was combined with all new available material for comparisons. All measurements showed significant differences (P < 0.01) among species according to t-tests.
Morphometric differentiation within the subgenus Artibeus
Differentiation among species was assessed by discriminant analysis. Canonical axes 1, 2, and 3, derived from the 9 cranial variables, accounted for 57.2%, 21.2%, and 16.4% of the interspecific variation, respectively (Table 2). A plot of canonical axes 1 and 2 (Fig. 2A) showed a poor craniometrical differentiation among most species, with A. anthonyi occupying an intermediate position in overall size among the large species of Artibeus. However, when canonical axes 1 and 3 were plotted (Fig. 2B), we observed the separation of A. anthonyi along the y axis. This 3rd canonical variate had a high negative correlation with the variables width of the rostrum across the m2s, and width of the postorbital constriction (Table 2), indicating the lowest values of both cranial variables toward the top of the plot.
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Fig. 2 Plots of scores of A) canonical variates 1 versus 2, and B) canonical variates 1 versus 3 obtained from discriminant function analysis of 9 cranial variables from 9 species of the subgenus Artibeus.
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Table 2 Correlations between canonical variates (CVs) and 9 cranial variables selected for comparisons of recent species of the genus Artibeus and the extinct Artibeus anthonyi.
Unweighted pairgroup method using arithmetic averages clustering showed that A. anthonyi is well distinguished from the 8 other species of Artibeus (Fig. 3). The Cuban fossil showed the greatest values of cranial divergence in terms of Mahalanobis distance with respect to other Artibeus species (Table 3). The greatest morphological divergence occurred between A. anthonyi and A. planirostris (D2 = 47.6), followed by that between A. anthonyi and A. obscurus (D2 = 44.8). A. anthonyi showed the least divergence from A. amplus (D2 = 19.3).
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Fig. 3 Dendrogram constructed employing the unweighted pairgroup method using arithmetic averages based on Mahalanobis distances for 9 species of the subgenus Artibeus.
table
Table 3 Morphometric divergence between species of Artibeus examined as indicated by Mahalanobis distances (D2).
Discussion
Based on morphological similarities, Phillips et al. (1989) speculated that A. schwartzi from St. Vincent is a relictual population of A. anthonyi. Pumo et al. (1996), noting the supposed morphological similitude between A. anthonyi and A. planirostris, hypothesized that A. anthonyi represents an early arrival to the Antilles of A. planirostris, and that it lost its taxonomic identity through hybridization with A. jamaicensis. These hypotheses do not gain further support when considered in light of our results. Among all species of the subgenus Artibeus we found the 2nd greatest cranial divergence between A. anthonyi and A. planirostris (exceeded only by the difference between A. anthonyi and A. obscurus). Although A. anthonyi exhibits similarity to A. planirostris in some craniometrical characters, these species (and maybe A. schwartzi) differ in their cranial appearance. Likewise, we found little or no morphometric overlap between A. anthonyi and samples of the extant A. jamaicensis from Cuba. Other elements, such as the doubtful coexistence of A. anthonyi and A. jamaicensis in the Cuban Holocene (see below) and the lack of large Artibeus fossils from Cuba and other islands north of St. Vincent (Morgan 2001), do not support the hybridization hypotheses. On the other hand, Larsen et al. (2007) included A. j. trinitatis in the phylogenetic species A. planirostris. Guerrero et al. (2004) found high molecular divergence between triomylus and jamaicensis and suggested full species rank for triomylus. These molecular studies indirectly support the presence–absence of M3 as a diagnostic character for the separation between Antillean and continental species.
That A. anthonyi shows a high cranial divergence from extant mainland Artibeus and that it was geographically restricted to Cuba suggest that it could be an ancient lineage within Artibeus. To date, hypotheses about the South American origin of A. anthonyi have prevailed (Phillips et al. 1989; Pumo et al. 1996; Woloszyn and Silva 1977), but dispersal routes from Mexico or Central America, or both, to Cuba also have been proposed for stenodermatine bats (Koopman 1989). These hypotheses can be tested by inferring phylogenetic relationship among extant and fossil taxa.
Radiocarbon dates made directly on fossil material of A. anthonyi are unavailable today. However, samples of bones from 2 fossil deposits that include remains of A. anthonyi formed by the accumulation of barn owl (Tyto alba) pellets have been dated. One of these deposits gave ages ranging from 20,050 to 21,474 years ago (Suárez and Díaz-Franco 2003). The 2nd deposit yielded an age of 7,864 ± 96 years ago (Jiménez et al. 2005); however, because of the nature of this deposit the date could not reliably predict the age of the remains of A. anthonyi at the site.
Fossil specimens of A. anthonyi are commonly found in Quaternary cave deposits throughout Cuba, demonstrating that this species had a widespread distribution on the island. The extinction of A. anthonyi may have been caused by climatic changes that occurred in the late Pleistocene or early Holocene (see Curtis et al. 2001). Similar to other extinct Cuban stenodermatines (i.e., Phyllops vetus, P. silvai, and Cubanycteris silvai), a change to a drier climate in the Holocene could have caused changes in the distribution and abundance of resources such as fruits, strongly impacting these tree-dwelling bats. In recent time, populations of arboricolous bats on West Indian islands have been reduced after these islands were impacted by hurricanes (Gannon and Willig 1994; Pedersen et al. 1996). No evidence exists about the effect of competition by A. jamaicensis on the decline or extinction of populations of A. anthonyi as suggested by Woloszyn and Silva (1977). Strong evidence, such as molecular data, and the lack of specimens of A. jamaicensis in fossil deposits from some islands, suggests that A. jamaicensis recently invaded the Antilles across the Yucatan Channel into Cuba or Jamaica during the late Pleistocene, after the West Indies acquired their present form (Genoways et al. 2005; Larsen et al. 2007; Morgan 1989, 2001). Probably, at the time that A. jamaicensis reached Cuba, populations of A. anthonyi were declining or extinct. To date, there are no data supporting the coexistence of both species of Artibeus on Cuba. Anthony (1919) found some specimens of the “large form” (A. anthonyi) encrusted with lime, whereas the remaining Artibeus in the deposit “were in a loose earthy formation and had not become cemented.” Likewise, in other deposits where A. anthonyi has been recorded, no remains of A. jamaicensis were found (Jimenez et al. 2005; Suárez and Díaz-Franco 2003). In Cueva GEDA, preliminary observations on the fluorine content in bones of A. anthonyi and A. jamaicensis suggest that the former is older than the latter. In this deposit, specimens of A. anthonyi are more abundant than those of A. jamaicensis, whereas the opposite has been found in other deposits containing A. anthonyi (Woloszyn and Silva 1977). Unlike other Cuban deposits bearing the extinct Artibeus, Cueva GEDA certainly represents equivalence between the biocenosis and taphocenosis. Therefore, further taphonomic studies of the site should clarify questions related to the colonization and extinction of this species. On the other hand, DNA sequence from fossil material of A. anthonyi could help explain the origin and the phylogenetic relationships of the genus Artibeus throughout the Caribbean region.
Resumen
El subgénero Artibeus incluye 8 especies de murciélagos frugívoros de amplia distribución neotropical. La única especie fósil, Artibeus anthonyi, fue descrita de los depósitos Cuaternarios de Cuba, y su estado taxonómico ha sido controversial en la literatura. Con base en nuevo material fósil excepcionalmente bien preservado, una diagnosis enmendada de la especie y la descripción detallada del cráneo del murciélago fósil Artibeus son presentadas. A través de análisis multivariados exploramos la diferenciación morfométrica de A. anthonyi y las otras especies del subgénero Artibeus. El fósil cubano de Artibeus muestra la mayor divergencia morfológica entre los Artibeus existentes.
Acknowledgments
This project was supported by Zoological Collection Program of Instituto de Ecología y Systemática. We thank M. Condis, H. Farfán, L. D. Torres, C. Aldana, R. Rivera, and members of GEDA Group (Sociedad Espeleológica de Cuba) for direct assistance in the fieldwork. A. Hernández, W. Suárez, and G. Silva kindly provided fossil material for comparisons. Comments from 2 reviewers greatly improved the clarity of the manuscript.
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Appendix I
Specimens examined
Gazetteer of specimens and collecting localities of Artibeus jamaicensis parvipes and A. anthonyi. Provinces are listed in uppercase letters followed by specific localities, and latitude and longitude in paretheses. Specimens are deposited in the following collections: Zoological Collection of the Instituto de Ecología y Sistematica, Ciudad Habana (CZACC); past Collection of Instituto de Zoología, Academia de Ciencias de Cuba (IZ); and Paleontological Collection of Museo Nacional de Historia Natural de Cuba (MNHNCu).
Artibeus jamaicensis parvipes (fresh material)
PINAR DEL RÍO: Cueva del Indio, San Diego de los Baños (22°56′N, 82°57′W), CZACC 1. 2224, 1. 2228, 1. 2232. CIUDAD DE LA HABANA: El Laguito, Playa (23°05′N, 82°28′W), CZACC 1. 2221, 1. 2222; Quinta de los Molinos, Cerro [past Botanical Garden] (23°06′N, 82°23′W), CZACC 1. 2245. PROVINCIA HABANA: Cueva Cayamas, Isla de la Juventud (21°49′N, 82°42′W), CZACC 1. 2196, 1. 2201, 1. 2205, 1. 2208. MATANZAS: Cueva de Los Murciélagos, Bacunayagua (23°05′N, 81°20′W), CZACC 1. 2294; Cueva de Los Murciélagos, Jagüey Grande (22°30′N, 81°09′W), CZACC 1. 2189, 1. 2192; Cueva de Santa Catalina, Camarioca (23°05′N, 81°24′W), 1. 2292. CIENFUEGOS: Jardín Botánico, Soledad (22°07′N, 80°20′W), CZACC 1. 2161, 1. 2162, 1. 2275, 1. 2276, 1. 2278; small cave beneath the road that passes over the Yaguanabo River (21°51′N, 80°13′W), CZACC 1. 2179, 1. 2180, 1. 2182, 1. 2184. SANCTI SPIRITUS: Cueva de Los Murciélgos, Sierra de Esperanza (22°01′N, 79°27′W), CZACC 1. 2297. CAMAGÜEY: Cueva Ñico López, Esmeralda (21°51′N, 78°06′W), CZACC 1. 2172; Cueva Maraguán, Camagüey (21°21′N, 77°45′W), CZACC 1. 2256. HOLGUÍN: Cueva Estrada, El Almirante (20°56′N, 76°11′W), CZACC 1. 2163, 1. 2165. SANTIAGO DE CUBA: Embalse Chalons, Santiago de Cuba (20°04′N, 75°49′W), CZACC 1. 2274; Cueva de la Cantera, Siboney (19°58′N, 75°43′W), CZACC 1. 2212, 1. 2216, 1. 2218, 1. 2268, 1. 2269.
Artibeus jamaicensis parvipes (fossil or subfossil material)
PINAR DEL RÍO: Cueva GEDA, Viñales (22°39′N, 83°42′W), [skulls] CZACC 26. 1941, 26. 1942. CIUDAD HABANA: Cueva de la Santa, Bacuranao (23°11′N, 82°12′W), [skull] CZACC 26. 1943. SANCTI SPIRITUS: Cueva Grande, Punta Judas (22°23′N, 79°00′W), [skulls] CZACC 26. 1919, 26. 1920.
Artibeus anthonyi
PINAR DEL RÍO: Cueva GEDA, Viñales (22°39′N, 83°42′W), [skull + mandibles] CZACC 26. 1933, 26. 1934, 26. 1937, 26. 1938; [skull] CZACC 26. 1935, 26. 1936, 26. 1939, 26. 1940; Cueva El Abrón, Los Palacios (22°40′N, 83°28′W), [skulls] MNHNCu 76. 4652–76. 4665. PROVINCIA HABANA: Cueva Paredones, Ceiba del Agua, Caimito (22°52′N, 82°38′W), [skull] CZACC 26. 1900. SANCTI SPIRITUS: quarry in a limestone hill near Moza, 5 km NE from Sancti Spiritus (21°57′N, 79°25′W), [skull] CZACC 26. 1891 [IZ-344.5, paratype]; Cueva del Centenario de Lenin, Punta Judas (22°21′N, 79°00′W), [skulls] CZACC 26. 1888 [IZ-344.2, holotype], 26. 1889 [IZ-344.3, paratype], 26. 1890 [IZ-344.4, paratype]; Cueva Grande, Punta Judas (22°21′N, 79°00′W), [skulls] CZACC 26. 1911–26. 1918, 26. 1921–26. 1925; [mandibles] CZACC 26. 1893 [IZ-344.6], 26. 1926–26. 1929.
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