Emballonura atrata Peters, 1874

GOODMAN, STEVEN M., CARDIFF, SCOTT G., RANIVO, JULIE, RUSSELL, AMY L. & YODER, ANNE D., 2006, A New Species of Emballonura (Chiroptera: Emballonuridae) from the Dry Regions of Madagascar, American Museum Novitates 3538 (1), pp. 1-24 : 5-11

Emballonura atrata Peters, 1874

This taxon was described based on a single specimen collected ‘‘aus dem Innern von Madagascar’’ ( Peters, 1874: 694), or in the interior of Madagascar. The holotype, which has been examined in the Museum für Naturkunde, Humboldt Universität, Berlin, is cataloged as number 4692. The cadaver is in alcohol and the pelage faded in coloration. The extracted skull is in relatively good shape, although the premaxillaries and associated incisors are not attached, the zygomatic processes are not intact, the occipital and palatine bones are partially broken, and considerable soft tissue still remains in the alisphenoid and basisphenoid region and partially obscures these structures. A label glued to the bottle containing the specimen has written upon it ‘‘4692 ♀, Emballonura atrata Ptrs. Madagaskar Crossly’’ and no date is associated with the specimen. The collector is undoubtedly Alfred Crossley, a British natural historian who visited Madagascar on several occasions, and obtained specimens particularly in the eastern portion of the island that are deposited in numerous European collections ( Tattersall, 1986; Dorr, 1997). There is no evidence that he traveled to drier western portions of the island, particularly areas of deciduous forest. It has been previously suggested that J. M. Hildebrandt collected the E. atrata holotype ( Peterson et al., 1995, footnote, p. 56), which is not correct.

Further evidence that the holotype specimen of E. atrata comes from the eastern humid forests is that, within the same accession at the Berlin Museum as specimen 4692, there are a variety of other mammal specimens, such as the lipotyphlan Hemicentetes and the primates Propithecus diadema and Lichanotus mitratus [5 Indri indri ] that represent taxa of this biome. Crossley collected the holotype of L. mitratus in the northern portion of Madagascar in the region of ‘‘Nossi Vola und Saralalan’’ ( Peters, 1871). This site has been interpreted by Schwarz (1931) as probably from the Lalo River, east of the Bay of Antongil. If this is indeed the case, the site is close to the modern city of Maroantsetra. Another possibility is that the site of ‘‘Nossi Vola’’ is Nosivola (17 ° 439S, 48 ° 399E), which is located to the east of Lac Alaotra and on the road between Ambatondrazaka and Manakambahiny-Est. What is almost certain is this material would have been collected on his late 1869 expedition to Madagascar, when Crossley disembarked at Vohemar and collected in various portions of the eastern humid forest and the region of Lac Alaotra ( Grandidier, 1872; Tattersall, 1986). Using the above-presented information, we restrict the type locality to the ‘‘lowland regions of the northern portion of eastern Madagascar.’’

On the basis of details presented below, we have examined specimens of a large and dark form of Emballonura that are assigned to E. atrata from the region of Maroantsetra south to Tolagnaro and covering much of the eastern portion of the island (fig. 1; appendix 1). All of these specimens come from lowland sites or the lower end of the montane zones (less than 900 m) and we are unaware of any evidence of this species in the Central Highlands. After comparison of our recently collected specimens of Malagasy Emballonura from several different sites, as well as older museum material, to the holotype of E. atrata , it is evident that an undescribed species exists in the drier northern and western portions of the island. This conclusion is corroborated by genetic analyses of the mitochondrial cyt b gene and D-loop region.

Emballonura tiavato , new species

Figures 2 , 3 , 4 , 5 , Table 1, Appendices 2, 3

HOLOTYPE: Field Museum of Natural History number 169705, adult male prepared as skin, skull, and partial postcranial skeleton (original number 11923a), collected January 22, 2001, by S. M. Goodman.

The study skin is in a good state of preservation, with both wings folded under the body and the tail membrane spread. The skull is intact with the delicate premaxillaries still attached and the rami of the mandible separated. Portions of the postcranial skeleton were also saved. The habitat noted on the specimen label is ‘‘In dry deciduous forest at base of tsingy ’’; this latter word from the Malagasy refers to a particular type of eroded limestone formation. The individual was captured in a harp trap placed along a trail in the forest and within 40 m of the north entrance of Andrafiabe Cave. The collection site is a limestone karst area with an extensive underground cave system ( Cardiff and Befourouack, 2003).

External measurements noted on the specimen label are: total length— 64 mm, tail length— 15 mm, hind foot length (not including claw)— 5 mm, tragus length— 5 mm, ear length— 14 mm, and forearm length— 36 mm. The fresh body mass of the specimen was 3.7 g. The testes were abdominal, measured 2 X 1 mm, and the epididymes not convoluted.

TYPE LOCALITY: Madagascar: Province d’Antsiranana , Réserve Spéciale d’Ankarana, 2.6 km E of Andrafiabe, in forest near Andrafiabe Cave, 12 ° 55.99S, 49 ° 03.49E, ± 50 m.

ETYMOLOGY: The name tiavato is derived from the Malagasy and means ‘‘likes rocks’’. This refers to the propensity of this species to occur in areas with exposed rock outcrops and caves.

DIAGNOSIS: A diminutive species of Emballonura (forearm length 5 36–41 mm in males and 35–42 mm in females) with notably long rounded ears (11–15 mm in males and 12–15 mm in females). The dorsum pelage coloration is uniform pale to medium grayishbrown and the ventrum is paler buff-brown (fig. 2, left). Inner portion of tragus convex with distinct hatchet-shaped anterior projection. Calcar slightly shorter in length than tibia. Nasal bone hourglass shaped and with distinct central sulcus. Relatively narrow diastema between PM 1 and PM 2. Basisphenoid pits distinctly rounded and of medium depth and separated by median septum.

REFERRED SPECIMENS: See appendix 1.

DISTRIBUTION: Known from the drier portions of Madagascar, from the Daraina region inland from Vohemar north to Ankarana and then south along the western side of the island to at least Bemaraha (fig. 1). We have not examined a specimen of Emballonura reported from ‘‘Tuléar’’ [5 Toliara] ( Peterson et al., 1995), but we presume it to be referable to this species. Fieldwork in the Mikea Forest between Toliara and Morombe and to the south near Saint Augustin and Tsimanampetsotsa has not provided any evidence of the presence of this genus ( Goodman and Razakarivony, 2004; Goodman et al., 2005).

DESCRIPTION: Dorsum cover fur notably long and slightly shaggy, with slightly silky texture, and uniform pale to medium grayishbrown color: basal one-quarter notably lighter and approaching medium-gray in color. The ventrum is paler buff-brown, with a slightly grayish-brown cast: basal one-third distinctly lighter and medium-gray in color. Little anterior–posterior variation in dorsum or ventrum coloration. Pelage in E. atrata notably darker, approaching brownish-black on dorsum and ventrum (fig. 2, right).

Ears long (11–15 mm in males and 12– 15 mm in females), terminating with slightly pointed tip, but notably more acutely pointed in E. atrata (fig. 3). In E. tiavato , the inner portion of tragus convex with distinct hatchetshaped sharp anterior projection, and in E. atrata , this structure is distinctly less developed and more rounded (fig. 3). In E. tiavato , there is a distinct swelling at base of outer portion of tragus that is not present in E. atrata . On average calcar shorter than tibia in E. tiavato , while in E. atrata these two structures are approximately the same length.

Cranium notably small, distinct rostral expansion across the nasal and maxilla, and postorbital processes greatly reduced in size (fig. 4). Rostral width narrower with respect to E. atrata . In E. tiavato and E. atrata , postorbital crest not confluent with sagittal crest. Occipital portion of skull less inflated than in E. atrata . In E. tiavato , nasal bones are distinctly hourglass shaped and with welldefined, deep, and relatively broad nasal

179357) taken at Andavakoera; right, E. atrata (FMNH 178595) obtained near Midongy du Sud.

sulcus that terminates well before the anterior margin of the nasal (fig. 5). This is in contrast to E. atrata , in which the lateral edges of the nasal bones are largely in parallel, the nasal sulcus is less broad, and the anterior margin of the sulcus nearly reaches the superior edge of the nasal. E. tiavato has a relatively narrow diastema between PM 1 and PM 2, which is distinctly wider in E. atrata (fig. 4). Basisphenoid pits in E. tiavato of medium depth and separated by median septum as in E. atrata . The distal limit of the pit is rounded and in E. atrata more oblong in shape and extends distally toward the auditory bullae.

COMPARISONS: Other than Mosia , Emballonura is the only genus of Emballonuridae with the dental formula of 2/3-1/1–2/2-3/3. All adult specimens of Emballonura that we have examined from Madagascar possess this dental formula. Mosia , which is often placed as a subgenus of Emballonura , is notably different from Emballonura based on structural differences in the hyoid apparatus, tragus, and penis ( Griffiths and Smith, 1991; Griffiths et al., 1991).

Excluding E. atrata , of the eight species recognized in this genus (sensu Simmons, 2005), the following six have forearm lengths notably greater than that of the Malagasy species and are not included in the morphological comparisons below: E. furax Thomas, 1911 ; E. dianae Hill, 1956 ; E. alecto (Eydoux and Gervais, 1836) ; E. monticola Temminck, 1838 ; E. semicaudata (Peale, 1848) , and E. serii Flannery, 1994 ( Taylor, 1934; Flannery, 1994, 1995a, 1995b; Bonaccorso, 1998; Ingle and Heaney, 1992). The other two non-Malagasy Emballonura species can be distinguished from the species described herein, E. tiavato , by their multicolored dorsal pelage with distinctly white under fur ( E. raffrayana Dobson, 1879 ), notable differences in tail and hind foot length ( E. beccarii Peters and Doria, 1881 , E. raffrayana ; appendix 2), distinct rostral swelling ( E. beccarii , E. raffrayana ), and anterolateral extension of basisphenoid pits and absence of median septum between the pits ( E. beccarii , E. raffrayana ).

The differentiation of E. tiavato and E. atrata is based on a suite of different characters. The primary distinguishing characters are pelage, ear tip shape, tragus shape, shape of nasals, PM 1 and PM 2 diastema width, and shape of basisphenoid pits (see Description section above). For immediate recognition of an individual in the hand, pelage and a few external characters can be used to separate these species. The dorsum pelage coloration of E. atrata is a distinctly monocolored blackish-brown to black, with a slightly lighter ventrum (fig. 2). In contrast, the dorsum of E. tiavato is a notably lighter uniform pale to medium grayish-brown and the ventrum is paler buffy-brown (fig. 2). In E. tiavato , the anterior lateral portion of the tragus has a distinct hatchet shape, as compared to the blunter tragus tip in E. atrata (fig. 3). Further, there is no overlap in adult body weight between E. tiavato (mean 5 3.6 g, range 2.7–4.5 g, N 5 37) and E. atrata (mean 5 5.3 g, range 5.0– 7.1 g, N 5 6; t 5 2.02, df 5 41, P 5 1.54 27)—these comparisons exclude pregnant females with moderate to large embryos.

To better evaluate differences in external measurements of these two taxa, we restricted our comparisons to specimens measured by the same field collector (SMG)—for E. tiavato these include specimens obtained at Ankarana (OTU 1) and for E. atrata those from Midongy du Sud (subset of OTU 2). With the exception of hind foot length, all of the mean external measurements made in the field of animals from these two populations were significantly different (table 1; appendix 2). For a suite of other variables, including other external (wing metacarpals and phalanges, tibia, and calcar), cranial, and dental measurements, we compared all of the adult individuals of OTUs 1, 3, and 4 (5 E. tiavato ) against those of OTU 2 ( E. atrata ). In these cases, significant differences were found between E. tiavato and E. atrata in body weight, all wing bone measurements, tibia, calcar, and all of the cranial-dental measurements, with the exception of C 1 –C 1 (table 1; appendix 3).

Given the ambiguity associated with the exact locality where the holotype of E. atrata

TABLE 1 Selected Measurements of Combined Adult Male and Female Emballonura tiavato and E. atrata a was obtained, it was critical to associate this species name with one of the two distinct species of this genus occurring on Madagascar. On the basis of numerous external, cranial, and dental characters, the name atrata is applicable to the larger and darker eastern species. The holotype of E. atrata (ZMB 4692) is distinctly faded in coloration, which is not unexpected after well over 130 years in alcohol. However, in his description of E. atrata, Peters (1874) noted dark pelage coloration, matching that of eastern members of this genus. Further, Dorst (1947), in a key to the bats of Madagascar, noted that the pelage of E. atrata was uniformly blackish.

A principal component analysis was conducted on a series of cranial measurements available for the holotype of E. atrata , and these were compared to individuals from the four different OTUs. The first two factors of the analysis explained 83.5% of the variance, and greatest zygomatic breadth, mastoid width, and rostral width had heavy loadings (table 2). When the scores of these two factors are plotted against one another (fig. 6), there is a clear separation between populations occurring in the humid forest formations (OTU 2) and dry forest formations (OTUs 1, 3, and 4). Further, the holotype of E. atrata (ZMB 4692) falls within the scatter of points associated with the humid forest formations, providing further evidence that this population is referable to this species.

TAXONOMIC NOTE: To our knowledge, the only name previously used for a species of Emballonura on Madagascar is E. atrata

TABLE 2 Factor Loadings of Principal Component Analysis for Selected Cranial Measurements Available from the Slightly Damaged Holotype of Emballonura atrata and Compared to Specimens from All Four OTUs a

Peters, 1874. The exception is the mention of E. madagascariensis by Sclater (1864), which we consider a nomen dubium.

CORROBORATING GENETIC RESULTS

Phylogenetic and network analyses show that regional sampling sites are well differentiated. The three samples of Emballonura from Midongy du Sud, in southeastern Madagascar, have identical haplotypes at both the cyt b and D-loop loci. Alternatively, network analyses of both loci reveal that the southeastern haplotype is the most divergent among all sampled Malagasy Emballonura , being at least six mutations removed at the D-loop (fig. 7) and at least 20 mutations removed at the cyt b locus (fig. 8).

Analyses of molecular variance confirm the patterns of regional genetic structure observed in the network analyses. Malagasy Emballonura samples are significantly structured between northern and western (5 E. tiavato ) and southeastern ( E. atrata ) regions, with 68.83% of the variance at the cyt b locus found between the two regions (ϕ ST 5 0.688; P, 0.001) and 69.08% of the variance at the Dloop found between the two regions (ϕ ST 5 0.690; P, 0.001).

An intriguing variant is seen in FMNH 173002, a specimen of E. tiavato from the Réserve Spéciale d’Ankarana. This individual is morphologically indistinguishable from its conspecifics, yet is genetically more similar to E. atrata at both mitochondrial loci examined here. We consider this to be a result of incomplete lineage sorting acting on the nonrecombining mitochondrial genome, and may indicate a relatively recent time since the divergence of these two species.

Overall, we find evidence of two distinctive groups of Emballonura on Madagascar. The observed genetic patterns are consistent with the presence of multiple demes, but due to the low sampling size and the lack of geographically intermediate sampling sites, we cannot exclude simple isolation by distance as a viable hypothesis based solely on genetic data. However, the totality of the evidence, considering these genetic patterns in light of the morphological and distributional data, strongly support the existence of a previously undescribed species in the dry areas of northern and western Madagascar.

Figures

Fig. 2. Color photographs of the two species of Emballonura known from Madagascar. Left, holotype of E. tiavato (FMNH 169705) obtained near the Andrafiabe Cave in the Réserve Spéciale d’Ankarana (photograph courtesy of Harald Schütz); right, specimen of E. atrata (FMNH 178595) captured in the central humid forest in the vicinity of Midongy du Sud (photograph by Steven M. Goodman). Note difference in pelage coloration between the two species.

Fig. 3. Comparison of ear and tragus structures in Malagasy Emballonura spp. Left, E. tiavato (FMNH

Fig. 4. Dorsal, ventral, and lateral views of adult crania and mandibles of Malagasy Emballonura spp. Left, holotype of E. tiavato (FMNH 169705; greatest skull length to canines 5 13.0 mm) from near Andrafiabe Cave, Réserve Spéciale d’Ankarana, from the dry deciduous forests of northern Madagascar; right, E. atrata (FMNH 178595) from near Midongy du Sud, from the eastern humid forests of southeastern Madagascar.

Fig. 5. Dorsal view of rostral portion of Malagasy Emballonura spp. Left, holotype of E. tiavato (FMNH 169705) from near Andrafiabe Cave, Réserve Spéciale d’Ankarana; right, E. atrata (FMNH 178595) from near Midongy du Sud. Note the difference in the shape of the nasal bones between the two species.