Late Pleistocene Bat Fossils from Anjohibe Cave, Northwestern Madagascar

Acta Chiropterologica, 9(1): 39–65, 2007 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS

Late Pleistocene bat fossils from Anjohibe Cave, northwestern Madagascar

KAREN E. SAMONDS

Redpath Museum, McGill University, 859 Sherbrooke St. W., Montréal, Québec H3A 2K6, Canada E-mail: [email protected]

In spite of decades of research on Madagascar’s unique and endemic modern fauna, the evolutionary history of the island’s bat fauna remains largely unknown. Their origin and evolution is largely unknown because of the nature of the fossil record; the deepest well-dated glimpse of Madagascar’s mammal groups comes from only 26,000 years ago. Bat remains have frequently been recovered from paleontological sites, but have been rarely identified or described. It therefore remains unknown whether bats underwent a reduction in species diversity similar to that seen in many of Madagascar’s vertebrate clades. Herein I describe a collection of newly discovered subfossil bats from Anjohibe Cave, northwestern Madagascar, some estimated to have been deposited about 80,000 years ago. Five bat genera are represented as subfossil (Rousettus, Eidolon, Hipposideros, Triaenops, and Myotis) with four of these genera present in Anjohibe Cave today. The subfossil material has yielded two new species, indicating that Malagasy bats experienced recent species turnover, paralleling what is seen in much of the island’s terrestrial vertebrate fauna.

Key words: Madagascar, subfossil, Chiroptera, Anjohibe Cave, Late Pleistocene

INTRODUCTION (Simons et al., 1995). A diverse subfossil fauna has been described from Holocene Madagascar’s extant fauna is one of the deposits, including crocodyliforms, turtles, most unique and endemic on the planet giant lemurs, bats, carnivorans, pigs, ro- (Goodman and Benstead, 2005), and ex- dents, pygmy hippos, the aardvark-like ploring the circumstances leading to the Plesiorycteropus, and birds (e.g., Godfrey modern distribution of its animals has been et al., 1990; Burney et al., 1997; Gommery the focus of decades of scientific research. et al., 2003; Goodman et al., 2004). More However, in spite of these efforts, the evo- than 30 subfossil localities are presently lutionary history of the island’s bats, per- recognized on Madagascar, and are largely haps the least-studied of Madagascar’s ex- distributed in the western and southern por- tant mammals, has remained poorly known. tions of the island, with a few in the north Present knowledge regarding the evolu- and on the Central High Plateau (Godfrey et tionary history of modern Malagasy mam- al., 1999; Burney et al., 2004). During the mals is based on subfossils (referring to end of the 19th and first third of the 20th their geologically shallow age), with our century, an emphasis was placed on the col- first glimpse at a mere ≈ 26,000 years BP lection of larger fossils such as primates, 40 K. E. Samonds hippos, carnivorans, and elephant birds; that these extinctions, occurring approxi- while bat remains have been recovered from mately 2,000 to 500 years BP, likely post- subfossil sites, they have seldom been iden- dated the arrival of humans (Burney, 1999, tified or described (Sabatier and Legendre, 2003; Burney et al., 1997, 2003, 2004), es- 1985; Ravoavy, 1986; Burney et al., 1997). timated at approximately 2,300 years BP As of May 2007, 37 species of extant (Burney et al., 2004; Perez et al., 2005). bats are presently recognized in Madagas- Herein I report on a diverse assemblage car, ≈ 60% of which are endemic (Eger of newly discovered bat fossils from An- and Mitchell, 2003; Goodman and Cardiff, johibe Cave, northwestern Madagascar; 2004; Goodman et al., 2005a, 2005b, some of this material is estimated to have 2006a, 2006b, In press; Bates et al., 2006). been deposited approximately 80,000 years As more concentrated collecting efforts are ago. This is more than three times the age of made, new species of Malagasy bats are still the oldest described Cenozoic vertebrate being discovered at a high rate (e.g., Good- subfossils, providing a deeper glimpse into man and Cardiff, 2004; Goodman et al., this gap and the evolutionary history of 2005a, 2006a, 2006b, In press). Malagasy bats. Madagascar’s present assemblage of vertebrate species, while exceptionally MATERIALS AND METHODS unique, represents only a subset of the diversity known from the island’s recent geo- Study Site logical past. Multiple extinction events during the Holocene exterminated nearly all of Anjohibe Cave, also known in the literature as Tsinjomitondraka or Grottes d’Andranoboka, is locat- Madagascar’s large-bodied native animals ed in the southern part of the current dry savannah of (MacPhee, 1986; MacPhee and Marx, 1997; the Mahavo plains in northwestern Madagascar, Burney, 1999). Radiocarbon dates suggest northeast of Mahajanga (Decary, 1934; Burney et al.,

FIG. 1. Anjohibe Cave, northwestern Madagascar. Breccia localities are shown in small black stars on the Anjohibe Cave detail map. Adapted from de Saint-Ours and Paulian (1953) and Burney et al. (1997). Map scale in meters Malagasy subfossil bats 41

1997 — Fig. 1). The caves at Anjohibe are part of a karst cave system formed within the Eocene lime- stone plateau (Besairie, 1956). Anjohibe (‘big cave’ in Malagasy) consists of a large cave system with an underground river running in the southeastern portion (de Saint-Ours and Paulian, 1953; Burney et al., 1997), and several extant animals inhabiting the cave, . (2004) . (2004) including bats. The region has undergone extensive et al human modification, and subfossil representation of et al arboreally adapted groups (e.g., sloth lemurs) suggests that this region was considerably more forested in the past. Fossils frequently occur in accumulations be- neath dolines (large sinkholes) or skylights (openings in the ceiling), as animals fall through these from the surface. Within the cave interior, some fossils are also concentrated into bone breccias, collections of bone fragments and sediment cemented together with min- eral deposits. Breccias demonstrate a large range of depositional processes; some fossils appear to have

been slowly trapped within forming speleothems, Comments Source while others appear to have been transported large distances by subterranean streams, and subsequently deposited and consolidated. The breccia samples used in this study were collected from four localities in Anjohibe Cave (Fig. 1 and Table 1). In some cases, these samples contained high concentrations of bat bones (Fig. 2).

Uranium-Series Dating Lat/Long 46°53.17’E100 m collapsed-cave feature 46°53.17’E100 m cave deposit Breccia samples were dated at Florida State 46°53.09’E 222 m University using Uranium-series (230Th/234U) techniques on the flowstone intercalated with the bone breccia layers. Speleothems were sampled and ana- lyzed according to standard dating techniques (e.g., Brook et al., 1990; Burney et al., 1994, 2004). Age estimate 10,000 kyr BP10,000 kyr BP – – Collapsed cave region Collapsed cave region pers. comm., 2001 A. Burney, D. pers. comm., 2001 A. Burney, D. Fossil Preparation ≤ ≤ > ? kyr 15°32.39’S Collected near cave entrance pers. comm., 2001 A. Burney, D. 1 1 2 The breccias containing these fossils were collected in 1996 by the team of Dr. David Burney, and Dating accessed into the collections of the Département de method /Elevation Paléontologie et Anthropologie Biologique, Univer- sité d’Antananarivo, Madagascar (UA). Fossils were extracted from breccia matrix using standard acetic acid preparation techniques (Toombs and Rixon, 1959; Grant, 1989; Leiggi and May, 1994; Lindsay, 1995).

Species Identification 1.Anjohibe Cave Age determinations based on U-series analysis for breccia samples collected from The osteological terminology and measurements ABLE OLD SE Speleothem U-series NCC-1 #4 Speleothem U-series 86.8 ± 7.8 kyr BP 15°32.55’S Laminated stalagmite on floor of Burney NCC-1 #3 Speleothem U-series 69.6 ± 7.3 kyr BP 15°32.55’S Directly below bone breccia in collapsed- Burney Provenance Material used herein follow Hershkovitz (1971), Sigé et al. TW-10SS2 Speleothem U-series Surface block U-series T 42 K. E. Samonds

(1982), Hand (1993, 1998), Freeman (1998), and Sa- sizes were judged too small, including cases where monds (2006). A large comparative sample of pho- there was only one specimen in a group, one-sample tographs, epoxy dental casts, and measurements of t-tests were enlisted to evaluate ‘group’ differences, modern Malagasy bats was collected to facilitate or whether or not the sample value belonged to the identification, focusing when possible on specimens larger, given ‘population’. collected from Anjohibe Cave (Samonds, 2006). In addition, collections of non-Malagasy bats were pho- Anjohibe Cave Breccia Localities tographed and measured to aid in interpreting material that did not match modern taxa known from the is- OLD SE Locality land. Measurements were made with 500-172 Mitu- The OLD SE samples were collected 13 August toyo digital calipers to 0.01 mm, or with an MA285 1996 from a collapsed area that blocked a long, dead- Meihi Techno optical reticule X, 1/100 (0.01 mm). end passage extending southeastward from one of the cave’s largest caverns (Fig. 1). Dating indicates that Quantitative Methods the four samples collected were approximately 10,000 years old or younger (D. A. Burney, pers. comm., When sample sizes were adequate, discriminant 2003; see Table 1). function analysis was used to examine potential group differences and degrees of group overlap. This analy- TW-10 Locality sis (SPSS 11.0) includes a multivariate analysis of Breccia samples were recovered from the TW-10 variance to test for significant differences among des- locality, approximately 60 m north of Entrance V1 (de ignated groups (e.g., Wilks’ lambda for the overall Saint-Ours and Paulian, 1953), and located on the analysis as well as subsets of the discriminant axes). southeast side of the subterranean river (Fig. 1). The percentage variance explained by each axis is re- Dating indicates that these samples were approxi- ported, and classification results pinpoint any individ- mately 10,000 years old or younger (D. A. Burney, ual ‘misclassified’ to another group. When sample pers. comm., 2003; see Table 1).

FIG. 2. Anjohibe Cave breccia sample TW-10, illustrating density of bones and teeth Malagasy subfossil bats 43

NCC-1 Locality Guinea and off east Africa (Simmons, The breccia samples from NCC-1 were collected 2005). The species E. dupreanum is endem- from deep within Anjohibe Cave in an open-air ic to Madagascar (Peterson et al., 1995). fissure (Fig. 1). Dating indicates that NCC-1 is the oldest of the dated bone breccias estimated as 69,600 to 86,800 years old (Burney et al., 2004; Table 1). Eidolon dupreanum (Schlegel 1867)

SS2 Locality Referred Specimens Unlike the other three samples, which were exca- Two left distal humeri (UA 8995, 8996), vated from the cave interior, the SS2 sample was col- two right proximal radii (UA 8997, 8998), lected from the surface, near the main cave entrance sub-adult left maxilla with C1 and P3 in (Fig. 1). Dating attempts revealed that this sample crypts (UA 8999), isolated left P4, upper in- was contaminated by detrital thorium, not meeting cisor, and P , and right C , P , and P4 (UA the ‘closed system’ required for successful U-series 3 1 2 dating (Table 1). 9000–9005), partial posterior braincase (UA 9006), right scaphocentralolunate (UA Abbreviations Used in Text 9007), left partial scapula (UA 9008). Institutions Description AMNH — American Museum of Natural History, Both left distal humeri (UA 8995, 8996) New York; FMNH — Field Museum of Natural possess a short trochlea, a capitulum with History, Chicago; MCZ — Museum of Compara- a relatively low and domed central surface tive Zoology, Harvard University, Cambridge; MNHN — Muséum National d’Histoire Naturelle, and a short, squared off lateral surface, and Paris; ROM — Royal Ontario Museum, Toronto; a broad but low epitrochlea with a superior UA — Département de Paléontologie et Anthro- surface not exceeding the height of the pologie Biologique, Université d’Antananarivo, An- trochlea. Both right proximal radii (UA tananarivo; USNM — Smithsonian Institution, 8997–8998) possess broad expanded tips National Museum of Natural History, Washington, with shallow excavations for articulation D.C. with the humerus. The lateral edges contain deep lips that wrap a short distance anteri- Morphometrics MD = mesiodistal; BL = buccolingual; HT = orly and posteriorly, and the medial edges height. possess thin shelves. The immature jaw (UA 8999) consists of the anterior portion of a left maxilla with SYSTEMATIC PALEONTOLOGY alveoli for C1, P2, P3 and P4. The upper canine remains within the crypt and is partial- Locality: OLD SE ly erupted, P2 is missing, the crown of P3 can be seen partially formed within the Order Chiroptera Blumenbach 1779 crypt but has not yet passed the alveolar Family Pteropodidae Gray 1821 surface, and P4 is missing, with the posteri- Genus Eidolon Rafinesque 1815 or edge of the crypt broken. A number of other possibly associated Included Species and Distribution teeth of this skull were also recovered, in- 4 The genus Eidolon contains two recog- cluding a left P , upper incisor, and P3, and 4 4 nized species: E. helvum Kerr, 1792 and a right C1, P2, and P (UA 9000–9005). P E. dupreanum Pollen, 1866. Eidolon hel- (UA 9000, UA 9005) has a medial and vum is presently distributed from Senegal to lateral ridge, with a shallow excavation be- Ethiopia and to South Africa, southwestern tween. The anterior aspect of the cusp has Arabia and Oman, and islands in the Gulf of a slight elaboration of the protocone, and 44 K. E. Samonds a lower but well-formed paracone. There is (13.70 and 13.47 mm, respectively) place a thin ridge connecting the two cusps medi- them near but outside the observed val- olaterally, and the posterior aspect of the ues of the modern Malagasy E. dupreanum crown is open between the medial and lat- (n = 4, 0 = 12.73 mm, SD = 0.36). One- eral ridges. The left upper incisor (UA sample t-tests suggest that both of these 9001) contains a single cusp terminating at measurements are significantly larger than a blunt point. P3 (UA 9004) has a tall, blunt in modern populations (P = 0.012 and cusp anteriorly, with a small posterior shelf, 0.025, respectively). However, extant male and a strong excavation on the posterior as- E. dupreanum are about 10% larger than pect of the cusp. C1 (UA 9002) is tall with females (MacKinnon et al., 2003) and, giv- a wide base, and possesses a thin groove en that none of the measured museum spec- on its anterior surface. P2 (UA 9003) has imens were of known sex determination, a short, wide crown with a single cusp on the possibility exists that this discrepancy in the anterolateral aspect. Only UA 9001 and size between fossil and modern specimens 9002 have any root formation; the remain- reflects differences in size dimorphism. ing teeth possess crowns with no roots. Based on this information, and the mor- The partial posterior braincase (UA phology of these elements, both are referred 9006) consists of the parietal and occipital to E. dupreanum. regions. UA 9006 has a poorly defined The proximal radii UA 8997 and 8998 sagittal crest and relatively well-developed are also referable to the family Pteropo- lambdoidal crest with posteriorly deflected didae based on their large size. The maxi- and thin paraoccipital processes. The brain- mum proximal radius width of UA 8997 case is superior-inferiorly compressed, and and 8998 (7.73 mm and 7.80 mm, respec- the foramen magnum is ovoid with elongat- tively) places them within observed values ed and well-developed occipital condyles. of modern Malagasy E. dupreanum (n = 4, The right scaphocentralolunate (UA 0 = 7.86 mm, SD = 0.378). One-sample 9007) is large, with a broad and flat proxi- t-tests suggest that neither of these speci- mal articular surface for its articulation with mens are significantly different from mod- the radius. The lateral distal surface con- ern populations (P = 0.54 and 0.77, respec- tains a large fossa for the trapezium, and tively). the medial aspect tapers to a narrow point. UA 8999 is referred to Pteropodidae The partial left scapula (UA 9008) con- based on the simple morphology and size of tains a narrow, shallow glenoid fossa, the teeth, as pteropodid teeth are highly a short, robust acromial process, and a rela- modified for frugivory and nectarivory tively longer and more slender coracoid (Bergmans, 1990), and frequently peg- process. shaped with little or no elaboration of the crown. As the isolated teeth (UA 9000– Comparison 9005) are unworn, their size and morphol- The three pteropodid bats presently in- ogy can be closely matched to those of habiting Madagascar are of dramatically modern Malagasy E. dupreanum. The different body size; from largest to smallest presence of this subadult in the deposits these are: Pteropus rufus (500–750 g), could indicate that the cave was used as E. dupreanum (235–346 g), and Rousettus a nursery colony for this taxon. Detailed madagascariensis (35–84 g) (Peterson et comparisons of maximum neurocranial al., 1995; Russ et al., 2001). The distal breadth and height are impossible due to humeral widths of UA 8995 and 8996 the fragmentary nature of specimen UA Malagasy subfossil bats 45

9006, but the broad shape and relative- the southwest (Sabatier and Legendre, 1985; ly large size of the partial braincase allows MacPhee, 1986). for identification of UA 9006 as E. dupreanum. Hipposideros sp. cf. H. commersoni While the morphology and articular relationships of the scaphocentralolunate are Referred Specimens similar in all bats (Stafford and Thorington, Left P4. 1998), UA 9007 is identified as pteropodid based on its extremely large size. Detailed Description statistical comparisons were not possible UA 9009 consists of a left P4 possessing due to the lack of comparative museum one main cusp anteriorly and a smaller pos- specimens, as bat postcrania (specifical- terior shelf. There is no anterolingual cusp ly isolated wrist and ankle bones) are ex- present, as in the case of several species of tremely rare. However, the length of this el- Hipposideros. The hypoconal basin is shal- ement (10.45 mm) appears to fall most ap- low. There is a low but distinct cingular heel propriately within the size range of the and a basal cingulum surrounds the major- medium-sized Malagasy fruitbat E. dupre- ity of the crown. The anterior aspect of the anum, because P. rufus has a substantially main cusp is convex anteriorly. larger scaphocentralolunate (14.25 mm, n = 2) and R. madagascariensis has a much Comparison smaller body size. The morphology of UA 9009 most The relatively simple morphology and closely resembles that of members of the large size of the scapula UA 9008, in ad- family Hipposideridae, which possess a P4 dition to the glenoid size (height = 7.29 mm, that is generally tall with a well-developed breadth 4.40 mm) places it within the ob- principal cusp, well-formed posterior shelf, served values of E. dupreanum (mean and shallow hypoconal basin. Within the height = 7.11 mm, SD = 0.36; mean breadth two genera of Hipposideridae presently on = 4.25 mm, SD = 0.32, in both cases n = 4). Madagascar, this tooth most closely match- One-sample t-tests suggest that both of es those of Hipposideros; representatives of these measurements are not significant from the other genus, Triaenops, are significantly modern populations (P = 0.40 and 0.43, smaller. Further support for this designation respectively). is the fact that H. commersoni is the only extant Malagasy non-pteropodid bat species comparable in size. The only other bat on Family Hipposideridae Lydekker 1891 Madagascar approaching the large size of Genus Hipposideros Gray 1831 H. commersoni is Mops midas (45 g — Fen- ton and Rautenbach, 1986), but this molos- Included Species and Distribution sid species has a P4 with a more flattened Hipposideros is a widely distributed anterior face, stronger lingual cingulum, genus that occurs throughout the Old World and taller main anterior cusp. tropics. The species H. commersoni is en- Although similar in overall tooth mor- demic to Madagascar (Simmons, 2005). phology, a one-sample t-test suggests that Subfossil H. commersoni have previously UA 9009 is significantly different from been reported from the younger deposits of modern H. commersoni, exhibiting larg- Anjohibe Cave (Burney et al., 1997) and er dimensions for mesiodistal length, from the Lake Tsimanampetsotsa region in buccolingual breadth, and height, and 46 K. E. Samonds subfossil H. besaoka sp. nov. (Table 2; Referred Specimens 4 see Locality: TW-10, below). Its P also Partial left dentary with M2–3 (UA 9011; lacks an anterolingual cusp (present in both Fig. 3C); partial right dentary with M2–3 extant H. commersoni and H. besaoka). (UA 9012; Fig. 3D). Based on the data presented here, UA 9009 is referred to Hipposideros sp. cf. H. com- Diagnosis mersoni, and considered distinct from both Larger than any known species of taxa. Triaenops. Molar crowns narrow, with protoconid and hypoconid more rounded labi- Genus Triaenops Dobson 1871 ally than seen in modern Triaenops species. M2 molar dimensions significantly longer Included Species and Distribution than in T. auritus, T. rufus, and T. furculus Species of Triaenops are widespread (P < 0.001). Protoconid only slightly taller throughout eastern Africa, Madagascar, the than hypoconid; in T. auritus, T. rufus, and coast of the Arabian Peninsula, and Aldabra T. furculus, the protoconid is noticeably Island. This genus is presently divided into taller than the hypoconid. Relative height of five species, with three of them endemic to paraconid, entoconid, and metaconid all Madagascar (T. auritus, T. furculus, and shorter than in T. auritus, but similar to T. rufus), one endemic to the Aldabra Island condition in T. rufus and T. furculus. (Triaenops nov. sp.), and one known only Molars lacking well developed preen- from Africa and parts of the Middle East tocristid between metaconid and entoconid. (T. persicus — Simmons, 2005; Ranivo and Talonid noticeably wider than talonid. Goodman, 2006; Goodman and Ranivo, In Molars containing small, labially expanded press). anterior and posterior cingula, and M2 containing small lingually expanded shelf be- Triaenops goodmani sp. nov. tween protoconid and hypoconid. (Fig. 3A–D) Description Etymology UA 9010 (Fig. 3A, B) is a partial left Specific name for Dr Steven M. Good- dentary containing P4M1–2. It is relatively man, in recognition of his significant contri- complete anteriorly, with alveoli for P2 and butions to the field of modern Malagasy bat the lateral incisor, but is broken posteriorly. research. P4 is approximately the height of the tallest cusp (paracone) of M1, or only slightly Type Specimen higher. The morphology is caniniform with Partial left dentary with P4M1–2 (UA one very tall median cusp lacking a mesial 9010; Fig. 3A–B). and buccal shelf. M1 is unworn, and has

TABLE 2. One-sample t-test results (2-tailed) for single Hipposideros P4 from OLD SE (UA 9009), compared to extant H. commersoni and subfossil H. besaoka from Anjohibe Cave (TW-10). Probability level: *** — P < 0.001 vs. H. commersoni vs. H. besaoka Character UA 9009 n 0 SD t-test n 0 SD t-test MD length of P4 2.12 40 1.99 0.145 -5.31*** 31 2.13 0.104 0.57 BL length of P4 2.40 40 2.14 0.132 -12.33*** 31 2.52 0.168 3.97*** HT P4 2.35 37 2.15 0.137 -8.79*** 27 2.18 0.152 -5.73*** Malagasy subfossil bats 47

1 mm

FIG. 3. Specimens of T. goodmani sp. nov. from OLD SE. A — UA 9010, labial view of type specimen of

T. goodmani sp. nov. partial left dentary with P4M1–2; B — UA 9010, occlusal view; C — UA 9011, lingual view of T. goodmani sp. nov. partial left dentary with M2,3; D — UA 9012, lingual view of T. goodmani sp. nov. partial right dentary with M2,3 a tall trigonid and only slightly lower ta- UA 9011 is a partial left dentary (Fig. lonid. The protoconid is the tallest cusp, and 3C) broken anterior to M2, but containing there is a well-developed but only slightly both M2 and M3, both of which are relative- shorter hypoconid. The paraconid and ento- ly worn. UA 9011 has a complete ascending conid are shorter than the hypoconid, but ramus and a relatively deep mandibular cor- approximate each other in height, while the pus. The morphology of M2 is the same as metaconid is slightly lower. The hypo- that seen in UA 9010. M3 also mirrors the conulid is the lowest cusp; it is noticeable overall morphology of the other molars, but but small. There is a distinct gap between is slightly smaller, and has no space be- the entoconid and hypoconulid, and no dis- tween the entoconid and hypoconulid. tinct ridge uniting the metaconid and ento- There is a weak ridge between the metaconid. M1 possesses a talonid wider than the conid and entoconid, which is deflected trigonid. M2 is comparable in morphology slightly labially; in both M1 and M2 this an- and size to M1, but contains a talonid only gle is more parallel to the toothrow. M3 pos- slightly wider than the trigonid. sesses a trigonid and talonid of equal width. 48 K. E. Samonds

UA 9012 is a partial right dentary con- separation between extant members of this

taining M2 and M3 (Fig. 3D), and consists genus (Samonds, 2006). When M2 (the of a partial ascending ramus with a relative- common tooth to UA 9010–9012) was

ly shallow mandibular corpus. M2 and M3 compared to each of the modern species us- are worn, but share the morphology de- ing one-sample t-tests, in all cases, subfos- scribed for UA 9011 and UA 9010. sil T. goodmani were significantly larger in mesiodistal dimensions than the three Comparison extant species (Table 3). UA 9010 and All three lower jaws (UA 9010–9012) 9011 were significantly different in bucco- share the specialized insectivorous bat mo- lingual width from both T. auritus and lar morphology of high cusped teeth and T. rufus, but not from T. furculus, although relatively robust mandibles (Freeman, UA 9012 was (P = 0.001). In a bivariate plot 1998). The size and molar morphology of of M2 measurements, T. goodmani cluster UA 9010–9012 most closely match those of in the upper portion of the range of T. furcu- Triaenops species. Triaenops is character- lus and T. rufus, with slightly longer molar

ized by having a P4 with a single main cusp dimensions (Fig. 4); T. furculus and T. rufus anteriorly with its mesial aspect in line with use Anjohibe Cave region today as a day

the mesial edge of the tooth. M1 and M2 roost site (Goodman et al., 2005b). How- possess a trigonid with tall and well-devel- ever, while subfossil Triaenops specimens oped protoconid, paraconid, and metaconid, fall outside the modern range for mesiodis- and a lower talonid posteriorly with a well- tal M2 dimensions, all three fall within the developed hypoconid buccally and a small modern range of measurements for buccol- entoconid and hypoconulid lingually with ingual dimensions (Fig. 4).

a distinct gap between. M3 is shorter in Previous analyses have suggested that length and possessing a short ridge between T. rufus is closely allied with T. persicus, the metaconid and entoconid, deflected and that T. auritus and T. furculus are dis- slightly labially. tinct from each other but closely related Discriminant function analyses of cra- (Peterson et al., 1995; Ranivo and Good- nial and dental measurements of mod- man, 2006). Recent genetic analyses also ern Triaenops species suggest suggests support these conclusions (Russell et al., that dental measurements provide the best 2007).

TABLE 3. One-sample t-test results for three specimens of T. goodmani from OLD SE (MD length and BL length of M2, respectively) compared to extant Malagasy species of Triaenops. Mean ± SD, and sample size (n) are also shown. Probability level: * — P < 0.05, *** — P < 0.001

T. goodmani T. auritus T. furculus T. rufus

MD length of M2 1.99 ± 0.145 (40) 2.13 ± 0.104 (31) 1.45 ± 0.055 (10) UA 9011: 1.57 16.62*** 9.96*** -6.75*** UA 9010: 1.55 14.11*** 8.23*** -5.60*** UA 9012: 1.57 16.62*** 9.96*** -6.75***

BL length of M2 2.14 ± 0.132 (40) 2.52 ± 0.168 (31) 0.95 ± 0.034 (10) UA 9011: 1.01 7.11*** 0.85 -5.41*** UA 9010: 1.02 5.88*** 0.31 -6.34*** UA 9012: 0.98 10.81*** 4.35*** -2.61* Malagasy subfossil bats 49

FIG. 4. Bivariate plot for mesiodistal and buccolingual dimensions of M2 for three extant Malagasy species of Triaenops (T. auritus, T. furculus, and T. rufus) and subfossil T. goodmani sp. nov. from OLD SE

Triaenops sp. Locality: TW-10

Referred Specimens Family Hipposideridae Lydekker 1891 Left distal humerus (UA 9200). Genus Hipposideros Gray 1831

Description Hipposideros besaoka sp. nov. UA 9200 is the distal half of a left hu- (Figs. 5A–C, 6A–D) merus possessing a well-developed trochlea and short broad epitrochlea. The central sur- Etymology The word besaoka (bay-SOH-ka) is de- face of the capitulum is displayed laterally rived from the Malagasy and means ‘big with the lateral surface of the capitulum ap- chin’. proximately the same size as the central portion, with a slight rounded expansion of Type Specimen its inferior aspect. Right maxilla with CP2,4M1–3 (UA 9478; Fig. 5A). Comparison The distal humeral width (3.58 mm) Diagnosis falls within the range of that observed for Larger and more robust than Hippo- the genus Triaenops. While the detail- sideros commersoni; similar to H. commer- ed morphology of the distal aspect of UA soni in possessing a great range of mandibu- 9200 most closely matches that of T. rufus, lar corpus depths and thickness (Figs. 5B the size difference between T. rufus and and 6C–D). Upper molars significantly T. goodmani is small, and this specimen broader, relative to length, than H. commer- could represent either species. soni (Figs. 5A and 6B). 50 K. E. Samonds

2 mm

FIG. 5. Hipposideros besaoka sp. nov. from TW-10, Anjohibe Cave, Madagascar. A — UA 9478, lingual view of type specimen, right maxilla with CP2,4M1–3 (P2 out of view); B — UA 9320, labial view of right dentary with

I1–2CP2,4M1–3; C — UA 9552, occlusal view of left dentary with I1–2CP2,4M1–3 Malagasy subfossil bats 51

Referred Specimens between premaxillae is thin with no crest on Twenty-six upper right maxillae (UA the dorsal surface. Each premaxilla houses 9284–9301, 9478, 9504–9511; Fig. 5A), 27 a single incisor, which is directed an- upper left maxillae (UA 9269–9283, teroventrally. Upper incisors are reduced 9512–9523; Fig. 6A–B), 78 left dentaries and weakly bilobed, with small flat crowns (UA 9232–9268, 9302–9319, 9330–9345, and thin roots that project minimally above 9497–9503, 9552; Fig. 6C–D), 40 right the alveolar line. dentaries (UA 9218–9231, 9320–9329, The maxillae (Figs. 5A and 6A–B) are 9481– 9496; Fig. 5B), 42 left and right pre- frequently well preserved, although many maxillae (UA 9346–9387), 26 isolated up- contain worn teeth. Maxillae possess upper per incisors (UA 9525, 9480 [lot of 25]), canines with one long principal cusp and 118 isolated lower incisors (UA 9526, a small posterior shelf approximately half- 9479 [lot of 117]), 41 upper left canines way up the posterior aspect of the tooth, ex- (UA 9398–9404, 9437–9470), 43 upper tremely reduced anterior upper premolar right canines (UA 9527, 9388–9397, (P2) wedged between the upper canine and 9405–9436), 26 lower left canines (UA P4, and a wide P4 with a tall anterior cusp, 9528 [lot of 26]), 25 lower right canines lower posterior shelf, and a well-defined an- 1 (UA 9530, 9529 [lot of 24]), 22 left P2 terolingual cusp. M has a closed protofossa (UA 9531, 9472 [lot of 17], 9550 [lot of 4]), with weak dihedral crest and a posteriorly 2 26 right P2 (UA 9551, 9471 [lot of 25]), deflected but low cingular heel. M is com- 2 right P4 (UA 9532, 9548), 4 left P4 parable to M1 but is squarer and slightly

(UA 9537, 9473, 9547 [lot of 2]), 1 right P4 smaller, with a less developed and posteri- 3 (UA 9539), 3 left P4 (UA 9538, 9549 [lot of orly deflected heel. M has an extremely re- 2]), 7 right M1 (UA 9543 [lot of 7]), 7 left duced W-pattern, where the premetacrista is M1 (UA 9474, 9545 [lot of 6]), 8 right less than 1/3 the length of the preparacrista, 2 1 M (UA 9476, 9477, 9544 [lot of 6]), 7 left and is significantly smaller (about /2) than M2 (UA 9475, 9546 [lot of 6]), 1 right M3 in both M1 and M2. (UA 9533), 3 left M3 (UA 9534 [lot of 3]), Lower jaws (Figs. 5B and 6C–D) show

18 right M1–2 (UA 9541 [lot of 18]); 13 left a large range of corpus depth and thickness, M1–2 (UA 9536 [lot of 4], 9542 [lot of 9]), with some extremely thin and shallow (UA 8 right M3 (UA 9540 [lot of 8]), 6 left M3 9244; Fig. 6C), and others robust and (UA 9535 [lot of 6]). deep (UA 9338; Fig. 6D). The dentary contains two small, anteroposteriorly com- Description pressed lower tricuspid incisors of approxi- The premaxillae rami were frequently mately the same size. The lower canine fused at the midline; these elements were has a single tall and narrow cusp. P2 is never found in association with skulls. large and moderately wide with a large main The posterior margin of the premaxilla cusp connected by steep crests to the ante- is narrowed to a thin point and flares rior and posterior edges of the crown, and gently anteriorly. The anterior margin ta- a smaller cusp posterior to the main cusp pers to a V-shape posteriorly between the within the posterior crest. P4 has two dis- incisors, which are located at the anterior- tinct roots, one tall median cusp, a tiny most edge near the tip of each anterolateral anterolingual cusp, and a small but well- projection. The ventral surface is concave developed posterolingual cusp. The post- longitudinally. Each premaxilla has a large erior ridge descending from the main cusp anterior palatal foramen. The line of contact consists of two parts; the first descending 52 K. E. Samonds weakly and the second turning more sharply protoconid is very tall and well-developed, inferiorly towards the posterolingual cusp. the metaconid is slightly lower, and the M1 is large, with a high trigonid and paraconid approximates the height of the relatively low talonid basin (Fig. 5C). The metaconid or surpasses it slightly. The

1 mm

FIG. 6. Specimens of H. besaoka sp. nov. from TW-10, Anjohibe Cave, Madagascar. A — UA 9272, labial view of left maxilla with CP2,4M1–3; B — UA 9272, lingual view of left maxilla with CP2,4M1–3; C — UA 9244, labial view of left dentary with CP2,4M1–2 and partial M3; D — UA 9338, labial view of left dentary with CP2,4M1–3 illustrating depth of mandibular corpus Malagasy subfossil bats 53 hypoconid is quite low. Both the anterior To compare subfossil Hipposideros and posterior cingula are weak, and the pro- specimens from Anjohibe to modern pop- toconid and hypoconid are at approximately ulations on the island, it was important the same distance from the midline of the to address the issue of latitudinal clines. tooth. The morphology of M2 mirrors that Hipposideros commersoni is broadly dis- of M1, and the size is comparable, or only tributed throughout Madagascar, encom- slightly smaller. The angle made by the pre- passing a wide range of habitats and tem- and postprotocristid is conspicuously nar- perature gradients. If modern groups dis- 3 rower in M2 and M than in M1. M3 is much play predictable relationships between shorter than M1 and M2 in mesiodistal size and latitude, the larger size of subfos- length, and has a greatly reduced talonid. sil Hipposideros might, at least in part, be The ridge between the metaconid and ento- attributable to changes in climate, as has conid is well developed but its posterior been previously demonstrated for bats else- margin is flexed laterally; the hypocristid is where in the Old World tropics (Storz et al., completely absent. 2001). Modern populations of H. commersoni Comparison from four distant regions of the island were For complete dentitions, the specimens compared to each other in an attempt to considered here are immediately referable address this issue. These four regions were to Hipposideros based in part on the dental divided into operational taxonomic units formula 1/2 1/1 2/2 3/3, the small upper (OTU’s) based on geography including premolar shifted laterally relative to the rest Analamerana, the northwest of the island of the toothrow (such that the canine and (including Anjohibe Cave, Mampikony, second upper premolar are in contact or and Ankarafantsika), Bemaraha, and Isalo nearly so), and the distinctive morphology (Fig. 10). Subpopulations of H. commer- of P2, being large and possessing a steeply soni do demonstrate significant differences sloped and broad buccal surface (Hand and between sites, with the most northern Kirsch, 1998, 2003). A Discriminant Func- (Analamerana) and the most southern tion Analysis of the Hipposideros fossils (Isalo) showing the closest relationship, and from TW-10 indicates that the subfossil the other two sites clustering discretely sample is significantly different than mod- (Fig. 10). ern H. commersoni (Fig. 7); H. besaoka up- Nevertheless, when six upper molar per molars are significantly broader (e.g., measurements available for the subfossil buccolingual dimensions) than seen in mod- sample are examined, and other extralim- ern H. commersoni (Fig. 8). ital species of Hipposideros that were for- Subfossil Hipposideros mandibles also merly considered subspecies of H. commer- show a large range of mandibular corpus soni are included, H. commersoni spec- depth and thickness sizes significantly imens group closely together, with the different from modern samples (Fig. 9). subfossils and extralimital species group- Overall, subfossil Hipposideros mandibles ing farther away (Fig. 11). This suggests have a thicker and more robust mandib- that the morphological differences be- ular corpus for their depth than modern tween the fossil specimens and extant Ma- H. commersoni, a morphology that, in mo- lagasy H. commersoni exceed the differ- lossid bats, has been correlated with spe- ences observed among the various extant cializations for hard-object feeding (Free- H. commersoni populations within Mada- man, 1981). gascar. 54 K. E. Samonds

Locality: NCC-1 the mesial lobe slightly smaller and the distal lobe smallest. It contains a single root

Hipposideros commersoni with a slight flare at its tip. UA 9202 is a M3 E. Geoffroy 1813 consisting of a complete crown with no roots preserved. The protoconid is tall and Referred Specimens well-developed, while the paraconid and Isolated lower incisor (UA 9201), right metaconid are relatively low. There is a M3 (UA 9202). well-developed crest (preentocristid) link- ing the metaconid to the entoconid, which is Description roughly parallel to the protocristid. The UA 9201 has a well-defined crown that trigonid is relatively wide. The talonid is ex- is trilobed and anteroposteriorly com- tremely reduced to a small shelf containing pressed. The central lobe is the largest, with a small hypoconid.

FIG. 7. Canonical discriminant function coefficients for Hipposideros from TW-10 and H. commersoni. A — upper molar measurements (M1MD, M1BL, M2MD, M2BL, M3MD, M3BL), Wilks’ lamba = 0.18, Chi-square

= 88.25, P < 0.001; B — lower molar measurements (M1MD, M1BL, M2MD, M2BL, M3MD, M3BL); Wilks’ lamba = 0.64, Chi-square = 54.07, P < 0.001. Line represents median, all outliers included Malagasy subfossil bats 55

FIG. 8. Bivariate plot for mesiodistal and buccolingual M1 molar dimensions for Hipposideros commersoni males and females, and subfossil H. besaoka from TW-10

Comparison Triaenops sp. The morphology and size of UA 9201 matches that seen in the modern form of Referred Specimens Hipposideros commersoni. UA 9202 shows Two left dentaries, one with P4M1 (UA the distinctive M3 morphology associated 9203), and one with M1–2 and part of a bro- with typical insectivorous bats, and is ken M3 (UA 9204). within the general size range of both the Malagasy Hipposideros and Mops midas Description miarensis. However, M. m. miarensis has UA 9203 is a well-preserved left dentary a slightly different M3 morphology, with with P4M1 intact. There is a small alveolus a more anteroposteriorly compressed trigo- for P2, but the jaw is broken anteriorly. The nid, and a preentocristid that does not par- posterior portion of the jaw is broken, and allel the protocristid, but rather forms the mandibular corpus depth is relatively a greater angle at its junction with the meta- shallow. A relatively large mental foramen conid. is present in line with the anterior aspect of An analysis of UA 9202 indicates that P4. P4 has a single tall median cusp, and is it is not statistically distinct from modern approximately the same height as the tallest H. commersoni, but is different from the cusp of M1 (paracone). M1 is unworn, and referred material of H. besaoka describ- possesses a relatively tall trigonid. The ed from locality TW-10 (Table 4). UA 9202 paraconid, entoconid, and metaconid are ap- is therefore referred here to H. commer- proximately the same height. The hypo- soni. conulid is small, and there is a distinct gap 56 K. E. Samonds

FIG. 9. Canonical discriminant function coefficients for Hipposideros from TW-10, measurements include corpus depth, corpus thickness, and ascending ramus height; Wilks’ lamba = 0.62, Chi-square = 74.77, P < 0.001. Line represents median, all outliers included between the entoconid and hypoconulid. M1 identical to that described for UA 9203, and also has a ridge between the metaconid the morphology of M2 mirrors that of M1. and entoconid. UA 9204 is a left dentary M3 is similar in morphology to the other with M1–2, a broken M3, and a shallow thin molars, but is slightly smaller, and has mandibular corpus. The M1 morphology is no space between the entoconid and

FIG. 10. Canonical discriminant function coefficients based on dental and mandibular measurements for four populations of Malagasy H. commersoni by site; % variance explained presented in parentheses. Measurements include mandible length, corpus depth, corpus thickness, ascending ramus height, P4MD, P4BL, M1MD, M1BL, 2 2 3 3 M MD, M BL, M MD, M BL, P4MD, P4BL, M1MD, M1BL, M2MD, M2BL, M3MD, M3BL, and M3HT Malagasy subfossil bats 57

FIG. 11. Canonical discriminant function coefficients for seven extant species previously recognized as subspecies of H. commersoni, and one extinct species (H. besaoka), based on mesiodistal and buccolingual molar dimensions (M1MD, M1BL, M2MD, M2BL, M3MD, M3BL). Closed solid symbols indicate H. commersoni organized by locality, subfossil H. besaoka indicated by (+), open symbols indicate non- Malagasy species previously within this species complex; % variance explained shown in parentheses hypoconulid. There is a small ridge between analysis. However, in an analysis of M1 di- the metaconid and entoconid, which is ori- mensions relative to the modern species ented slightly bucally; in both M1 and M2 (Fig. 12A–B), it appears that UA 9203 this ridge is more parallel to the toothrow. and 9204 are not immediately referable to T. goodmani since they cluster far from this Comparison species in both mesiodistal and buccolin- UA 9203 and 9204 most closely match gual dimensions. UA 9203 and 9204 also those of Triaenops species in size and over- possess a relatively strong ridge between all morphology. When the mesiodistal and the metaconid and entoconid; a character buccolingual dimensions of M1 (the tooth lacking in T. goodmani. Due to small sam- common to UA 9203 and 9204) were com- ple sizes, these two jaws are referred simply pared to those of each of the modern species to the genus Triaenops. of Triaenops using one-sample t-tests, the subfossil M1 were generally longer in me- Genus Rousettus siodistal length and smaller in buccolingual width than the four extant species of Triae- Included Species and Distribution nops for which post-cranial specimens are The genus Rousettus is distributed in available (Table 5). Due to a lack of com- Africa, Europe, Asia, Comoros, and Mada- parable specimens of T. goodmani (only gascar (Simmons, 2005); R. madagasca-

UA 9010 has an intact M1), it was not pos- riensis is endemic to Madagascar, and is sible to perform an adequate comparative the sole species of this genus present on the 58 K. E. Samonds

TABLE 4. One-sample t-test (2-tailed) results for Hipposideros sp. from NCC-1 compared to extant H. commersoni and subfossil H. besaoka from Anjohibe Cave (TW-10). Mean, SD, and sample size (n) are also shown. Probability level: *** — P < 0.001 vs. H. commersoni vs. H. besaoka Character UA 9015 n 0 SD t-test n 0 SD t-test

MD length of M3 2.23 40 2.22 0.127 -0.55 100 2.37 0.098 14.06*** BL length of M3 1.65 40 1.69 0.132 1.82 100 1.76 0.087 13.19***

island. It is presently distributed throughout simple and ‘rousettine’, but are also consid- the eastern rainforest, the deciduous forests erably narrow (Bergmans, 1977, 1994). UA of the west, southwest and north, and the 9206 appears to best match the morphology

Central High Plateau (MacKinnon et al., of M3, as this tooth lacks well-developed 2005). cusps, has a narrow width, and is short in length. Rousettus sp. cf. R. madagascariensis Locality: SS2 Referred Specimens

Right M3 (UA 9206). Hipposideros sp. cf. H. commersoni

Description Referred Specimens

UA 9206 consists of a partial tooth with Two isolated left M3 (UA 9207, 9208), part of its crown missing. The two roots are isolated left M1 (UA 9209), partial right

partially intact. The base of the crown is maxilla (UA 9210), right dentary with P4 very shallow and relatively broad. The an- (UA 9211), left dentary with isolated M1 terobuccal aspect of the crown is complete, (UA 9214), right P4 (UA 9213). and preserves a distinct ridge. Description

Comparison UA 9207 and 9208 are both left M3 con- Based on the small size and overall sisting of complete crowns with partial shape of the crown base and roots, UA 9206 roots intact. In both, the trigonid is relative- is assigned to the genus Rousettus, species ly wide and the protoconid and metaconid of which possess teeth that are typically are similar in height. The protoconid is

TABLE 5. One-sample t-test results for MD and BL lengths of M1 for Triaenops sp. from NCC-1. Malagasy species include T. auritus, T. furculus and T. rufus; T. persicus is distributed in Africa and the Middle East. Mean ± SD, and sample size (n) are also shown. Probability level: * — P < 0.05, ** — P < 0.01, *** — P < 0.001

Triaenops sp. T. auritus T. furculus T. rufus T. persicus MD length of M1 1.48 ± 0.046 (9) 1.46 ± 0.041 (15) 1.59 ± 0.057 (10) 1.56 ± 0.066 (6) UA 9016: 1.69 -13.64*** -22.00*** -5.33*** -4.80** UA 9017: 1.55 -4.50** -8.65*** 2.44* 0.44 BL length of M1 1.02 ± 0.039 (9) 0.99 ± 0.054 (15) 0.90 ± 0.048 (10) 0.94 ± 0.056 (6) UA 9016: 0.82 15.49*** 12.11*** 5.46*** 5.13** UA 9017: 0.85 13.21*** 9.95*** 3.49** 3.81* Malagasy subfossil bats 59 well-developed, and the talonid basin is ex- closed, and the large cingular heel is de- tremely reduced with a small hypoconid. flected posteriorly. The preentocristid is more or less parallel to The partial right maxilla, UA 9210, con- the protocristid. UA 9209 consists of a left tains P2,4M1–3. A large infraorbital foramen M1 crown with partial roots, but the hypo- lies superior to M1. P2 is vestigial and conal basin is broken. The protofossa is extremely reduced. It is displaced laterally

FIG. 12. Boxplots of mesiodistal and buccolingual dimensions of M1 for three extant Malagasy species of Triaenops (T. auritus, T. furculus, and T. rufus), subfossil Trianeops from NCC-1, and subfossil T. goodmani sp. nov. from OLD SE; A — mesiodistal dimensions; B — buccolingual 60 K. E. Samonds such that it is situated lateral to the anter- H. besaoka (Table 6), and combined with obuccal corner of P4. P4 has a tall, well- the small sample size, this makes assign- developed principal cusp, a relatively tall ment to species uncertain. posterior cusp, a tiny cingular cusp, and a shallow hypoconal basin. The lingual as- Rousettus madagascariensis pect of the crown has a relatively well- developed cingulum. M1 has a well-devel- Referred Specimen oped but low cingular heel. The paracone Distal right humerus (UA 9216). and metacone are the tallest cusps, followed by the parastyle, mesostyle, and metastyle Description respectively; the protocone is low. The UA 9216 is the distal end of a relatively paracrista and premetacrista are approxi- large right humerus, with a relatively well- mately equal in length and parallel to developed trochlea, and a flat broad capitu- each other, as are the postparacrista and lum. The shaft is extremely thin and the metacrista. The hypoconal basin is well- epitrochlea is flat and broad. The trochlea is developed and the heel is posteriorly de- low and steeply angled towards the junction flected. M2 is similar to M1, although it has with the epitrochlea, and the lateral surface a smaller hypoconal basin and less posteri- of the capitulum has a round excavation on orly deflected heel. M3 is substantially re- its lateral surface. duced in size, and has complete loss of the talonid, a medially displaced metaconid, Comparison and only the remnant of a heel. Pteropodid humeri are typically relative- UA 9211 is a right dentary with P4, ly simple and primitive, with less elabora- which has a tall median cusp and a shorter tion of the distal aspect than seen in other posterior cusp. The corpus is relatively deep bats. Based on the size and specific mor- and robust, and there are alveoli present phology of this specimen, UA 9216 is re- for P2, C and the lateral lower incisor. ferred to R. madagascariensis. UA 9214 consists of a left dentary with M . The ramus is broken and is relative- 1 Family Vespertilionidae Gray 1821 ly deep. M1 has a tall protoconid, slightly shorter hypoconid, and lower but approxi- Subfamily Vespertilioninae Gray 1821 mately equal paraconid and entoconid; the Genus Myotis Kaup 1829 lowest cusp is the hypoconulid. The trigonid is high while the talonid is low but com- Included Species and Distribution plete. Myotis is a very speciose and wide- UA 9213 is a right P4 with a large main spread genus, with 100 species presently cusp, a small posterior shelf, and a vestigial recognized (Simmons, 2005). Two subspe- anterolingual cusp. There is a low cingular cies of M. goudoti were previously recog- heel and the crown is surrounded by a basal nized: M. g. anjouanensis Dorst, 1960, cingulum. The hypoconal basin is shallow. restricted to Anjouan Island in the Como- ros and M. g. goudoti Dorst, 1960, endem- Comparison ic to Madagascar; both of these are now All of these specimens are referable recognized as distinct species (Simmons, to Hipposideros. However, the fact that 2005). Myotis goudoti inhabits most habitat UA 9207 and 9208 appear significantly types in Madagascar (Eger and Mitchell, different from both H. commersoni and 2003). Malagasy subfossil bats 61

TABLE 6. One-sample t-test results for Hipposideros rufus, R. madagascariensis, H. commer- from SS2 (M3) compared to extant H. commersoni soni, T. furculus, T. rufus, Miniopterus ma- and subfossil H. besaoka from Anjohibe Cave (TW- 10). Mean ± SD, and sample size (n) are also shown. navi, M. gleni, Myotis goudoti, and Oto- Probability level: * — P < 0.05, *** — P < 0.001 mops madagascariensis — Goodman et al., 2005; S. M. Goodman, pers. comm.). The Hipposideros H. commersoni H. besaoka sp. (TW-10) subfossils recovered from Anjohibe Cave indicate the presence of five genera, one of MD length of M3 2.22 ± 0.127 (40) 2.37 ± 0.098 (100) which (Eidolon) no longer inhabits this UA 9020: 2.32 -5.03*** 4.87*** cave system. Of the subfossil taxa identi- UA 9021: 2.27 -2.54* 9.97*** fied and described here, only four extant

BL length of M3 species (E. dupreanum, R. madagascarien- UA 9020: 1.63 2.77** 15.49*** sis, H. commersoni, and Triaenops sp. cf. UA 9021: 1.70 -0.57 7.44*** T. furculus) were previously recorded from the younger sediments of Anjohibe Cave Myotis goudoti (Burney et al., 1997); one is new for the site (M. goudoti). Furthermore, two of the Referred Specimen taxa identified are new and described here Lower right canine (UA 9217). (T. goodmani and H. besaoka). The large sample of subfossils referable Description to Hipposideros, its presence in all breccia UA 9217 is a very small isolated right samples, and the fact that species are also canine with a single tall pointed main cusp. commonly found in the younger sediments The lingual surface is spade-shaped and of the cave indicates that the genus was slightly concave. well represented in the overall cave fauna in the recent geological past. The only other Comparison record of Hipposideros from a subfossil de- UA 9217 matches the morphology and posit on the island is from Lake Tsimanam- size of M. goudoti. This species has unique petsotsa, southwestern Madagascar (Saba- small pointed canines with a single main tier and Legendre, 1985). cusp, and the unique lingual spade-shaped The evidence of a distinctly larger spe- surface, which is broad inferiorly. This cies of Hipposideros (H. besaoka) from isolated canine (1.47 mm) fits within TW-10 is especially significant, because the the modern size range seen in this species extant species H. commersoni is the largest (0 = 1.33, n = 3, SD = 0.076, one-sample insectivorous bat known from the island t-test, P = 0.083). (Russ et al., 2001). This new species has significantly wider molars than seen in DISCUSSION modern populations of H. commersoni, with a more robust and deeper mandibular Subfossil versus Modern Assemblages corpus. Although common as a breccia subfos- Of the subfossil bat specimens described sil, and extremely numerous within the in these breccia samples, all are attributable more recent Holocene deposits, Eidolon du- to genera represented on the island today. preanum is currently locally extinct in the Nine species of extant bats are known Anjohibe Cave system. This species has to use the Anjohibe Cave system as a day been recorded from many regions of Mad- roost based on a recent census (Pteropus agascar, but may be susceptible to human 62 K. E. Samonds pressures (Racey et al., 2002; MacKinnon extirpation (as seen in Eidolon) and island- et al., 2003). Roost sites appear to be espe- wide extinction as seen by T. goodmani and cially at risk; recent ecological studies sug- the largest known insectivorous bat on the gest that nearly half of the Eidolon roosts island, H. besaoka. It is also interesting to surveyed were deserted at least in part due note that the subfossil forms tend to be larg- to human hunting (Racey et al., 2002). In er than their extant relatives, although the many regions Eidolon is able to persist in difference is less than in other groups (e.g., deforested areas (MacKinnon et al., 2003). Cryptoprocta — Goodman et al., 2004; var- The extinction of Eidolon at Anjohibe ious lemur groups including Daubentonia appears to have occurred in the past few — Godfrey and Jungers, 2002). decades. Interviews with local villagers suggest that older adults recognize the ACKNOWLEDGMENTS bones of Eidolon as a ‘fanihy’ (fruit bat) that no longer occurs in the cave, but one I wish to thank the Government of Madagascar that lived previously in the cave system for permission to conduct research in Madagascar, during their childhood (S. M. Goodman, which was in collaboration with the Département de Paléontologie et Anthropologie Biologique, Univer- pers. comm.). The large quantity of Eidolon sité d’Antananarivo, Antananarivo. I also wish to bones on the surface of the cave floor also thank Drs. David Krause, William Jungers, Maureen supports a recent extinction event. O’Leary, Steven Goodman, Nancy Simmons, and It is interesting to note that not all spe- Mitchell Irwin. cies presently inhabiting the cave were de- Special thanks to financial support from the Cave Conservancy Foundation, Cave Research Foundation, tected as subfossils (e.g., Otomops, Minio- and the Field Museum of Natural History. I am grate- pterus). This may indicate that these genera ful to the museums and curators that helped to facili- colonized the cave more recently. However, tate this research, including Bill Stanley (FMNH), it is equally possible that they were not rep- Judith Chupasko (MCZ), Nancy Simmons, Bob resented in this sample due to chance or Randall, and Jean Spence (AMNH), Linda Gordon and Helen James (USNM), Judith Eger (ROM), taphonomic factors. Ronan Kirsch, Christiane Denys, and Marc Godinot (MNHN), and Armand Rasoamiaramanana and CONCLUSIONS GisPle Francine Noro Randria (UA). Thanks to the research team that collected and dated the Anjohibe Cave breccia, including David Caves are among the most delicate and Burney, Jim Cowart, Fred Grady, Helen James, and vulnerable ecosystems (Watson et al., 1997; William Jungers. I am grateful to Fred Grady van Beynen and Townsend, 2005), and are (USNM) for his instruction in acetic acid preparation particularly susceptible to human pressures. techniques, as well as the efforts of volunteer fossil Previous research has demonstrated a major preparators Kenneth Lee, Olivia van Nieuwenhuizen, loss of biodiversity in many of Madagas- Jennie Yu, and Jessica DeLalio, and to Colleen Lodge for her drawings of H. besaoka. Mitchell Irwin, car’s species during the Holocene (Godfrey Steven Goodman, and one anonymous reviewer pro- et al., 1990; Goodman, 1994; Burney et al., vided helpful comments on an earlier version of this 1997; Gommery et al., 2003), yet whether paper. Malagasy bats experienced similar extinctions has never been addressed. This paper LITERATURE CITED marks the first systematic study of subfossil Malagasy bats. BERGMANS, W. 1977. Notes on new material of Rousettus madagascariensis Grandidier, 1929 On the basis of subfossil remains re- (Mammalia, Megachiroptera). Mammalia, 41: covered within Anjohibe Cave, it is clear 67–74. that bats on the island experienced local BERGMANS, W. 1990. Taxonomy and biogeography of Malagasy subfossil bats 63

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Received 15 September 2006, accepted 12 December 2006