A New Species of Emballonura (Chiroptera - Yoder Lab

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY

CENTRAL PARK WEST A T 79TH STREET, NEW YOR K, NY 10024

Number 3538, 24 pp., 8 figures, 4 tables October 19, 2006

A New Species of Emballonura (Chiroptera:Emballonuridae) from the Dry Regions

of Madagascar

STEVEN M. GOODMAN,1,2 SCOTT G. CARDIFF,3 JULIE RANIVO,4

AMY L. RUSSELL,5 AND ANNE D. YODER6

ABSTRACT

We describe a new species of bat in the genus Emballonura (Chiroptera: Emballonuridae), E.tiavato, from the dry forest regions of Madagascar. This species is distinguished from the onlyother member of this genus found on the island, E. atrata, and extralimital species based ona variety of external and cranial characteristics. Details of the distribution, phylogeny, and naturalhistory of the two species of Malagasy Emballonura are presented.

RESUME

Une nouvelle espece de chauve-souris du genre Emballonura (Emballonuridae: Chiroptera), E.tiavato, des regions de forets seches de Madagascar est decrite ici. E. tiavato se distingue de E.

Copyright E American Museum of Natural History 2006 ISSN 0003-0082

1 Research Associate, Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History.2 Department of Zoology, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605

([email protected]) and WWF, BP 738, Antananarivo (101), Madagascar ([email protected]).3 Columbia University, Department of Ecology, Evolution, and Environmental Biology, 1200 Amsterdam Avenue, New

York, NY 10027; and Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History,([email protected]).

4 Departement de Biologie Animale, Universite d’Antananarivo, Faculte des Sciences, BP 906, Antananarivo (101),Madagascar and Ecology Training Program, WWF, BP 738, Antananarivo (101), Madagascar ([email protected]).

5 Department of Ecology and Evolutionary Biology, P.O. Box 208105, Yale University, New Haven, CT 06520-8105.Current address: Arizona Research Laboratories, 1041 E. Lowell St., BSW room 246b, Tucson, AZ 85721([email protected]).

6 Department of Ecology and Evolutionary Biology, P.O. Box 208105, Yale University, New Haven, CT 06520-8105.Current address: Departments of Biology & BAA, Duke University, Box 90338, Durham, NC 27708 ([email protected]).

atrata, seul autre membre appartenant a ce genre sur l’ıle, et de toutes les autres especes du memegenre au point de vue des caracteristiques externes et craniennes. La distribution, la phylogenie etl’histoire naturelle des deux especes d’Emballonura malgaches sont presentees en details dans cemanuscrit.

INTRODUCTION

The genus Emballonura (Family Emballo-nuridae) is broadly distributed from islands inthe western Pacific Ocean, through mainlandsoutheastern Asia and associated islands, toMadagascar. The latter island forms thewestern distributional limit of the genus. Ascurrently configured, Emballonura, often re-ferred to as a sheath-tailed bat, is composedof nine species (Simmons, 2005), of whicheight are only found on islands and sixare largely restricted to the Melanesianregion. The majority of Emballonura spp.have relatively restricted geographical distri-butions.

Two species of Emballonuridae are men-tioned in the literature as occurring onMadagascar—Emballonura atrata and Tapho-zous mauritianus—both known from specimenrecords across various portions of the island(Peterson et al., 1995; Goodman et al., 2005).A third species, Coleura afra, has been recentlydocumented for the island (Goodman et al., inpress). E. atrata, which is endemic toMadagascar, is previously recorded from veryfew sites and less than 30 specimens—nearlyone-half of these are fluid preserved or driedmummies with unextracted skulls. Thus, todate, insufficient material has been availableto examine patterns of geographic variation inthis species.

Over the past decade we have conducted batsurveys on Madagascar, particularly in the drywestern portion of the island. During thecourse of these inventories we have capturedindividuals of Emballonura at several sites,and, based on this new material, we are able toassess and quantify variation on a geographiclevel in members of this genus across much ofthe island. Contrary to early interpretations,Emballonura on Madagascar is widespread,rather than being restricted to the humidportions of the island (Honacki et al., 1982),and is not rare (Tate and Archbold, 1939),particularly in zones with exposed rock out-crops and caves.

MATERIALS AND METHODS

MORPHOLOGICAL ANALYSES

We have consulted specimens of adultEmballonura spp. housed in several naturalhistory museums. The acronyms of these insti-tutions are: AMNH American Museum ofNatural History, New York; FMNH Field Mu-seum of Natural History, Chicago; MNHNMuseum national d’Histoire naturelle, Paris,France; RMNH Naturalis, Leiden, The Nether-lands [formerly Rijksmuseum van NatuurlijkeHistoire]; ROM Royal Ontario Museum,Toronto, Canada; UADBA Universite d’Anta-nanarivo, Departement de Biologie Animale,Antananarivo, Madagascar; USNM NationalMuseum of Natural History, Washington, D.C.[formerly United States National Museum];ZMAK Zoologisches Museum Alexander Koe-nig, Bonn, Germany; and ZMB Museum furNaturkunde, Humboldt Universitat, Berlin,Germany [formerly Zoologisches Museum,Berlin].

We recorded five external measurements inmillimeters from captured individuals beforepreparation. These included: total length, taillength, hind foot length (not including claw),ear length, and forearm length. Further, wemeasured body mass in grams using a springbalance. For certain specimens, obtained byother collectors, measurement data were noteddirectly from labels or field catalogs held invarious museums. There are considerabledifferences among field collectors in thetechniques that they use to measure bats;most notable in this regard for emballonuridsis rather inconsistent methods for total length,tail, and hind foot measurements. Whentabulating descriptive statistics of externalmeasurements, we have in some cases onlyused those of a single collector—although thisreduces sample size, it also decreases the rangeand variance of external measurements. SMGalso took four wing and two hind limbmeasurements in millimeters from liquid pre-served specimens: total length of third digit(metacarpal), third digit (first phalanx), fourth

2 AMERICAN MUSEUM NOVITATES NO. 3538

digit (metacarpal), fourth digit (first phalanx),tibia, and calcar.

SMG measured seven cranial and fivedental characters using digital calipers, accu-rate to the nearest 0.1 mm. The measurementsand their definitions are: greatest skull lengthto canines: from posteriormost part of occip-ital to anterior-buccal alveolar border ofcanines; greatest zygomatic breadth: widthacross zygomatic arches at widest point;interorbital width: dorsal width at most con-stricted part of skull; mastoid width: greatestwidth across skull at mastoid processes;braincase height: from basiosphenoid andbasiooccipital bones to top of braincase (inMalagasy Emballonura the sagittal crest ispresent, but not well developed); rostral width:maximum width across rostrum dorsally atlacryimal protuberances; C1–C1: width acrossanterior-buccal alveolar border of canines;M1–M1: maximum width across palate atbuccal alveolar borders of third molars; andC1–M3: crown length from the anterior-buccalalveolar border of the canine to the posteriorbuccal margin of the third molar.

As some species of Emballonura show sexualdimorphism in size, with males being smallerthan females (Peterson et al., 1995;Bonaccorso, 1998), separate descriptive statis-tics were calculated for adults of each sex. Toassist with the analysis of patterns of geo-graphic variation in Malagasy Emballonura,particularly sites with small sample sizes, wehave grouped specimens as operational taxo-nomic units (OTUs) based on general regionof locality. These include the northern site ofAnkarana (OTU 1), all eastern sites south ofMaroantsetra (OTU 2), all western sites southof Nosy Be and Ambanja (OTU 3), and thenorthern sites of Daraina, Analamerana, andAndavakoera (OTU 4; fig. 1).

GENETIC ANALYSES

Our intention with the genetic analyses wasto assess whether they corroborated taxonom-ic conclusions drawn from the quantitativeand qualitative analyses. Total genomic DNAwas isolated using a DNeasy DNA isolationkit (Qiagen), and stored in the providedelution buffer. Approximately 250 bp of themitochondrial D-loop was amplified in E.

atrata using the primers F(mt) and Mt15996L(Wilkinson and Chapman, 1991; Campbell etal., 1995). The complete mitochondrial cyto-chrome b gene (cyt b) was amplified using theprimer pairs L14724/H15506 and L15171/UMMZ04 in E. atrata (Irwin et al., 1991;Yoder et al., 1996; Jansa et al., 1999). PCRswere performed in 50-ml reaction volumes,containing 2.25 mM MgCl2, 0.25 mM dNTPs,2.5 U Taq DNA polymerase, 5 ml Promega103 buffer, 5 ml genomic DNA, and 20 pmolof each primer. The amplification involved aninitial denaturation at 94uC for 3 min, fol-lowed by 40 cycles of 94uC for 45 sec, 52uC for45 sec, and 72uC for 1 min, with a finalelongation step at 72uC for 4 min. The PCRproduct was then purified using either gelband excision (Gel Excision kit, Qiagen) orPCR purification (PCR Purification kit,Qiagen).

The purified fragment was sequenced fromboth directions using the BigDye terminatorcycle sequencing kit v.3.1 (Applied Biosys-tems) in a 20-ml reaction containing 2 ml of theBigDye solution, 1.2 ml ABI 53 sequencingbuffer, 5 pmol of primer, and 100–200 ng ofpurified PCR product. The temperature profilewas conducted according to the manufacturer’sinstructions. The sequencing reactions werecleaned of unincorporated nucleotides usinggenCLEAN dye terminator removal plates(Genetix) and analyzed on an ABI3100 auto-mated sequencer. Each individual was se-quenced 4 to 15 times per locus from multiplePCR reactions to resolve any ambiguitiespresent in single sequencing passes. We usedSequencher v.4.2 (Gene Codes Corp.) to assem-ble and edit consensus sequences for eachindividual, and aligned the data by eye usingMacClade v.4.0 (Maddison and Maddison,2000). All sequences were deposited with Gen-Bank: cytochrome b (DQ178249–DQ178285)and D-loop (DQ178286–DQ178323).

We performed Bayesian and maximumparsimony phylogenetic analyses on the cytb data using MrBayes v.3.0b4 (Huelsenbeckand Ronquist, 2001) and PAUP* v.4.0b10(Swofford, 2002), respectively. Sequences ofSaccopteryx bilineata (Juste et al., 1999) andE. alecto (Hulva and Horacek, 2002) wereused as the outgroups. Maximum parsimonyanalyses were performed using heuristic

2006 GOODMAN ET AL.: NEW EMBALLONURA FROM MADAGASCAR 3

Fig. 1. Map of collection localities of Emballonura spp. on Madagascar and other sites mentioned in thetext. To the east of the north–south meandering line is Cornet’s (1974) ‘‘etage humide’’ or humid stage basedon his bioclimatic classification of the island.


searches with tree bisection–reconnection(TBR) branch swapping, and setting themaximum number of saved trees to 1000.Parsimony bootstrap analyses were performedusing heuristic searches, TBR branch swap-ping, and 100 replicates of the randomaddition search option. Bayesian analyseswere performed with flat priors, running fourchains of 10 million generations each, withsampling every 500 generations. The chainswere heated using the temperature scalingfactor T 5 0.2. We specified an HKY + Cmodel with four rate categories for the gammadistribution, the model having been specifiedusing ModelTest v.3.06 (Posada and Crandall,1998). After examining the likelihood profileusing Tracer v.1.1 (http://evolve.zoo.ox.ac.uk/software.html?id5tracer), we discarded thefirst 4000 trees as a burn-in and constructeda 50% majority consensus tree from theremaining 16,000 trees in PAUP* (Swofford,2002).

For each species and for each locus, we usedModelTest v.3.06 to determine the best-fittingmodel of evolution. Using the prescribedmodel and parameter values, we usedArlequin v.2.001 (Schneider et al., 2001) totest for genetic structure among geographicregions and sampling sites. We also usedDnaSP v.4.0 (Rozas et al., 2003) to calculatedescriptive measures such as haplotype di-versity (h) and nucleotide diversity (p).Parsimony networks were constructed foreach species and for each locus using TCSv.1.18 (Clement et al., 2000).

Emballonura atrata Peters, 1874

This taxon was described based on a singlespecimen collected ‘‘aus dem Innern vonMadagascar’’ (Peters, 1874: 694), or in theinterior of Madagascar. The holotype, whichhas been examined in the Museum furNaturkunde, Humboldt Universitat, Berlin,is cataloged as number 4692. The cadaver is inalcohol and the pelage faded in coloration.The extracted skull is in relatively good shape,although the premaxillaries and associatedincisors are not attached, the zygomatic pro-cesses are not intact, the occipital and palatinebones are partially broken, and considerablesoft tissue still remains in the alisphenoid andbasisphenoid region and partially obscures

these structures. A label glued to the bottlecontaining the specimen has written upon it‘‘4692 U, Emballonura atrata Ptrs. Mada-gaskar Crossly’’ and no date is associatedwith the specimen. The collector is undoubt-edly Alfred Crossley, a British natural histo-rian who visited Madagascar on severaloccasions, and obtained specimens particular-ly in the eastern portion of the island that aredeposited in numerous European collections(Tattersall, 1986; Dorr, 1997). There is noevidence that he traveled to drier westernportions of the island, particularly areas ofdeciduous forest. It has been previouslysuggested that J. M. Hildebrandt collectedthe E. atrata holotype (Peterson et al., 1995,footnote, p. 56), which is not correct.

Further evidence that the holotype speci-men of E. atrata comes from the easternhumid forests is that, within the same acces-sion at the Berlin Museum as specimen 4692,there are a variety of other mammal speci-mens, such as the lipotyphlan Hemicentetesand the primates Propithecus diadema andLichanotus mitratus [5Indri indri] that repre-sent taxa of this biome. Crossley collected theholotype of L. mitratus in the northernportion 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, eastof the Bay of Antongil. If this is indeed thecase, the site is close to the modern city ofMaroantsetra. Another possibility is that thesite of ‘‘Nossi Vola’’ is Nosivola (17u439S,48u399E), which is located to the east of LacAlaotra and on the road between Ambaton-drazaka and Manakambahiny-Est. What isalmost certain is this material would have beencollected on his late 1869 expedition toMadagascar, when Crossley disembarked atVohemar and collected in various portions ofthe eastern humid forest and the region of LacAlaotra (Grandidier, 1872; Tattersall, 1986).Using the above-presented information, werestrict the type locality to the ‘‘lowlandregions of the northern portion of easternMadagascar.’’

On the basis of details presented below, wehave examined specimens of a large and darkform of Emballonura that are assigned to E.atrata from the region of Maroantsetra south


to Tolagnaro and covering much of theeastern portion of the island (fig. 1; appen-dix 1). All of these specimens come fromlowland sites or the lower end of the montanezones (less than 900 m) and we are unaware ofany evidence of this species in the CentralHighlands. After comparison of our recentlycollected specimens of Malagasy Emballonurafrom several different sites, as well as oldermuseum material, to the holotype of E. atrata,it is evident that an undescribed species existsin the drier northern and western portions ofthe island. This conclusion is corroborated bygenetic analyses of the mitochondrial cytb gene and D-loop region.

Emballonura tiavato, new species

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

HOLOTYPE: Field Museum of NaturalHistory number 169705, adult male preparedas skin, skull, and partial postcranial skeleton(original number 11923a), collected January22, 2001, by S. M. Goodman.

The study skin is in a good state ofpreservation, with both wings folded underthe body and the tail membrane spread. Theskull is intact with the delicate premaxillariesstill attached and the rami of the mandibleseparated. Portions of the postcranial skeletonwere also saved. The habitat noted on thespecimen label is ‘‘In dry deciduous forest atbase of tsingy’’; this latter word from theMalagasy refers to a particular type of erodedlimestone formation. The individual wascaptured in a harp trap placed along a trailin the forest and within 40 m of the northentrance of Andrafiabe Cave. The collectionsite is a limestone karst area with an extensiveunderground cave system (Cardiff andBefourouack, 2003).

External measurements noted on the spec-imen label are: total length—64 mm, taillength—15 mm, hind foot length (not includ-ing claw)—5 mm, tragus length—5 mm, earlength—14 mm, and forearm length—36 mm.The fresh body mass of the specimen was3.7 g. The testes were abdominal, measured 23 1 mm, and the epididymes not convoluted.

TYPE LOCALITY: Madagascar: Provinced’Antsiranana, Reserve Speciale d’Ankarana,2.6 km E of Andrafiabe, in forest near

Andrafiabe Cave, 12u55.99S, 49u03.49E, 650 m.

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

DIAGNOSIS: A diminutive species ofEmballonura (forearm length 5 36–41 mm inmales and 35–42 mm in females) with notablylong rounded ears (11–15 mm in males and12–15 mm in females). The dorsum pelagecoloration is uniform pale to medium grayish-brown and the ventrum is paler buff-brown(fig. 2, left). Inner portion of tragus convexwith distinct hatchet-shaped anterior projec-tion. Calcar slightly shorter in length thantibia. Nasal bone hourglass shaped and withdistinct central sulcus. Relatively narrow di-astema between PM1 and PM2. Basisphenoidpits distinctly rounded and of medium depthand separated by median septum.

REFERRED SPECIMENS: See appendix 1.DISTRIBUTION: Known from the drier por-

tions of Madagascar, from the Daraina regioninland from Vohemar north to Ankarana andthen south along the western side of the islandto at least Bemaraha (fig. 1). We have notexamined a specimen of Emballonura reportedfrom ‘‘Tulear’’ [5Toliara] (Peterson et al.,1995), but we presume it to be referable to thisspecies. Fieldwork in the Mikea Forest be-tween Toliara and Morombe and to the southnear Saint Augustin and Tsimanampetsotsahas not provided any evidence of the presenceof this genus (Goodman and Razakarivony,2004; Goodman et al., 2005).

DESCRIPTION: Dorsum cover fur notablylong and slightly shaggy, with slightly silkytexture, and uniform pale to medium grayish-brown color: basal one-quarter notably lighterand approaching medium-gray in color. Theventrum is paler buff-brown, with a slightlygrayish-brown cast: basal one-third distinctlylighter and medium-gray in color. Littleanterior–posterior variation in dorsum orventrum coloration. Pelage in E. atratanotably darker, approaching brownish-blackon dorsum and ventrum (fig. 2, right).

Ears long (11–15 mm in males and 12–15 mm in females), terminating with slightlypointed tip, but notably more acutely pointed


in E. atrata (fig. 3). In E. tiavato, the innerportion of tragus convex with distinct hatchet-shaped sharp anterior projection, and in E.atrata, this structure is distinctly less devel-oped and more rounded (fig. 3). In E. tiavato,there is a distinct swelling at base of outerportion of tragus that is not present in E.atrata. On average calcar shorter than tibia inE. tiavato, while in E. atrata these twostructures are approximately the same length.

Cranium notably small, distinct rostralexpansion across the nasal and maxilla, andpostorbital processes greatly reduced in size(fig. 4). Rostral width narrower with respectto E. atrata. In E. tiavato and E. atrata,postorbital crest not confluent with sagittalcrest. Occipital portion of skull less inflatedthan in E. atrata. In E. tiavato, nasal bones aredistinctly hourglass shaped and with well-defined, deep, and relatively broad nasal

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

Fig. 3. Comparison of ear and tragus structures in Malagasy Emballonura spp. Left, E. tiavato (FMNH179357) taken at Andavakoera; right, E. atrata (FMNH 178595) obtained near Midongy du Sud.


sulcus that terminates well before the anteriormargin of the nasal (fig. 5). This is in contrastto E. atrata, in which the lateral edges of thenasal bones are largely in parallel, the nasalsulcus is less broad, and the anterior margin ofthe sulcus nearly reaches the superior edge ofthe nasal. E. tiavato has a relatively narrowdiastema between PM1 and PM2, which isdistinctly wider in E. atrata (fig. 4). Basis-phenoid pits in E. tiavato of medium depthand separated by median septum as in E.atrata. The distal limit of the pit is roundedand in E. atrata more oblong in shape andextends distally toward the auditory bullae.

COMPARISONS: Other than Mosia, Embal-lonura is the only genus of Emballonuridaewith the dental formula of 2/3-1/1–2/2-3/3. Alladult specimens of Emballonura that we have

examined from Madagascar possess this den-tal formula. Mosia, which is often placed asa subgenus of Emballonura, is notably differ-ent from Emballonura based on structuraldifferences in the hyoid apparatus, tragus, andpenis (Griffiths and Smith, 1991; Griffiths etal., 1991).

Excluding E. atrata, of the eight speciesrecognized in this genus (sensu Simmons,2005), the following six have forearm lengthsnotably greater than that of the Malagasyspecies and are not included in the morpho-logical comparisons below: E. furax Thomas,1911; E. dianae Hill, 1956; E. alecto (Eydouxand Gervais, 1836); E. monticola Temminck,1838; E. semicaudata (Peale, 1848), and E. seriiFlannery, 1994 (Taylor, 1934; Flannery, 1994,1995a, 1995b; Bonaccorso, 1998; Ingle and

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 nearAndrafiabe Cave, Reserve Speciale 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 ofsoutheastern Madagascar.


Heaney, 1992). The other two non-MalagasyEmballonura species can be distinguished fromthe species described herein, E. tiavato, bytheir multicolored dorsal pelage with distinctlywhite 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 swell-ing (E. beccarii, E. raffrayana), and antero-lateral extension of basisphenoid pits andabsence of median septum between the pits(E. beccarii, E. raffrayana).

The differentiation of E. tiavato and E.atrata is based on a suite of differentcharacters. The primary distinguishing char-acters are pelage, ear tip shape, tragus shape,shape of nasals, PM1 and PM2 diastemawidth, and shape of basisphenoid pits (seeDescription section above). For immediaterecognition of an individual in the hand,pelage and a few external characters can beused to separate these species. The dorsumpelage coloration of E. atrata is a distinctlymonocolored blackish-brown to black, witha slightly lighter ventrum (fig. 2). In contrast,the dorsum of E. tiavato is a notably lighteruniform pale to medium grayish-brown andthe ventrum is paler buffy-brown (fig. 2). In E.tiavato, the anterior lateral portion of thetragus has a distinct hatchet shape, ascompared to the blunter tragus tip in E. atrata

(fig. 3). Further, there is no overlap in adultbody weight between E. tiavato (mean 5 3.6 g,range 2.7–4.5 g, N 5 37) and E. atrata (mean5 5.3 g, range 5.0–7.1 g, N 5 6; t 5 2.02, df 541, P 5 1.5427)—these comparisons excludepregnant females with moderate to largeembryos.

To better evaluate differences in externalmeasurements of these two taxa, we restrictedour comparisons to specimens measured bythe same field collector (SMG)—for E. tiavatothese include specimens obtained at Ankarana(OTU 1) and for E. atrata those fromMidongy du Sud (subset of OTU 2). Withthe exception of hind foot length, all of themean external measurements made in the fieldof animals from these two populations weresignificantly different (table 1; appendix 2).For a suite of other variables, including otherexternal (wing metacarpals and phalanges,tibia, and calcar), cranial, and dental measure-ments, we compared all of the adult individ-uals of OTUs 1, 3, and 4 (5 E. tiavato) againstthose of OTU 2 (E. atrata). In these cases,significant differences were found between E.tiavato and E. atrata in body weight, all wingbone measurements, tibia, calcar, and all ofthe cranial-dental measurements, with theexception of C1–C1 (table 1; appendix 3).

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

Fig. 5. Dorsal view of rostral portion of Malagasy Emballonura spp. Left, holotype of E. tiavato (FMNH169705) from near Andrafiabe Cave, Reserve Speciale d’Ankarana; right, E. atrata (FMNH 178595) fromnear Midongy du Sud. Note the difference in the shape of the nasal bones between the two species.


TABLE 1

Selected Measurements of Combined Adult Male and Female Emballonura tiavato and E. atrataa

E. tiavato E. atrata

Total length 59.2 6 3.34 65.0 6 3.46

55–64, N 5 13 63–69, N 5 3

Tail length 16.0 6 1.28 18.7 6 1.15

15–18, N 5 12 18–20, N 5 3

Hind foot length 5.6 6 0.51 6.0 6 0.00

5–6, N 5 13 6–6, N 5 3

Ear length 12.5 6 0.88 16.3 6 2.31

11–14, N 5 13 15–19, N 5 3

Forearm length 37.2 6 1.69 40.3 6 0.58

35–41, N 5 13 40–41, N 5 3

Body mass 3.3 6 0.40 5.9 6 1.10

2.7–3.8, N 5 13 5.0–7.1, N 5 3

3rd digit–metacarpal 31.9 6 1.15 32.7 6 1.26

29.8–34.0, N 5 37 29.0–35.3, N 5 26

3rd digit–1st phalanx 14.3 6 0.53 14.8 6 0.59

12.9–15.3, N 5 37 13.6–16.1, N 5 26

4th digit–metacarpal 24.5 6 1.11 25.2 6 0.96

22.7–26.3, N 5 37 22.7–27.1, N 5 25

4th digit–1st phalanx 8.9 6 0.42 9.2 6 0.36

8.1–9.8, N 5 37 8.7–10.0, N 5 24

Tibia 15.4 6 0.77 15.8 6 0.72

13.1–16.7, N 5 39 14.8–17.5, N 5 24

Calcar 14.2 6 0.84 15.7 6 0.63

12.3–16.4, N 5 39 14.8–16.9, N 5 21

Greatest skull length to canines 13.0 6 0.36 13.3 6 0.29

12.2–13.6, N 5 40 12.8–13.8, N 5 13

Greatest zygomatic breadth 7.5 6 0.17 7.8 6 0.27

7.0–7.8, N 5 38 7.4–8.4, N 5 15

Interorbital width 2.5 6 0.14 2.7 6 0.13

2.3–2.8, N 5 41 2.4–2.9, N 5 20

Mastoid width 6.8 6 0.17 7.2 6 0.17

6.4–7.2, N 5 41 6.7–7.4, N 5 18

Braincase height 6.2 6 0.19 6.4 6 0.19

5.8–6.5, N 5 37 6.1–6.8, N 5 14

Rostral width 5.5 6 0.14 5.8 6 0.23

5.1–5.7, N 5 40 5.3–6.2, N 5 16

C1–C1 3.3 6 0.11 3.3 6 0.23

3.1–3.5, N 5 40 3.0–3.7, N 5 17

M1–M1 5.6 6 0.13 5.7 6 0.21

5.4–5.9, N 5 40 5.4–6.0, N 5 19

C1–M3 4.9 6 0.13 5.1 6 0.10

4.7–5.2, N 5 41 4.9–5.3, N 5 20

a External measurements are limited to a single field collector. For certain variables these two species exhibit sexual

dimorphism or subtle geographic differences that are presented in greater detail in appendices 2 and 3.


was obtained, it was critical to associate thisspecies name with one of the two distinctspecies of this genus occurring on Mada-gascar. On the basis of numerous external,cranial, and dental characters, the name atratais applicable to the larger and darker easternspecies. The holotype of E. atrata (ZMB 4692)is distinctly faded in coloration, which is notunexpected after well over 130 years in alco-hol. However, in his description of E. atrata,Peters (1874) noted dark pelage coloration,matching that of eastern members of thisgenus. Further, Dorst (1947), in a key to thebats of Madagascar, noted that the pelage ofE. atrata was uniformly blackish.

A principal component analysis was con-ducted on a series of cranial measurementsavailable for the holotype of E. atrata, andthese were compared to individuals from thefour different OTUs. The first two factors ofthe analysis explained 83.5% of the variance,and greatest zygomatic breadth, mastoidwidth, and rostral width had heavy loadings(table 2). When the scores of these two factorsare plotted against one another (fig. 6), thereis a clear separation between populationsoccurring 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 pointsassociated with the humid forest formations,providing further evidence that this popula-tion is referable to this species.

TAXONOMIC NOTE: To our knowledge, theonly name previously used for a species ofEmballonura on Madagascar is E. atrata

Peters, 1874. The exception is the mention ofE. madagascariensis by Sclater (1864), whichwe consider a nomen dubium.

CORROBORATING GENETIC RESULTS

Phylogenetic and network analyses showthat regional sampling sites are well differen-tiated. The three samples of Emballonura fromMidongy du Sud, in southeastern Mada-gascar, have identical haplotypes at both thecyt b and D-loop loci. Alternatively, networkanalyses of both loci reveal that the south-eastern haplotype is the most divergent amongall sampled Malagasy Emballonura, being atleast six mutations removed at the D-loop(fig. 7) and at least 20 mutations removed atthe cyt b locus (fig. 8).

Analyses of molecular variance confirm thepatterns of regional genetic structure observedin the network analyses. Malagasy Embal-lonura samples are significantly structuredbetween northern and western ( 5 E. tiavato)and southeastern (E. atrata) regions, with68.83% of the variance at the cyt b locusfound between the two regions (wST 5 0.688; P, 0.001) and 69.08% of the variance at the D-loop found between the two regions (wST 50.690; P , 0.001).

An intriguing variant is seen in FMNH173002, a specimen of E. tiavato from theReserve Speciale d’Ankarana. This individualis morphologically indistinguishable from itsconspecifics, yet is genetically more similar toE. atrata at both mitochondrial loci examinedhere. We consider this to be a result ofincomplete lineage sorting acting on thenonrecombining mitochondrial genome, andmay indicate a relatively recent time since thedivergence of these two species.

Overall, we find evidence of two distinctivegroups of Emballonura on Madagascar. Theobserved genetic patterns are consistent withthe presence of multiple demes, but due to thelow sampling size and the lack of geograph-ically intermediate sampling sites, we cannotexclude simple isolation by distance as a viablehypothesis based solely on genetic data.However, the totality of the evidence, consid-ering these genetic patterns in light of themorphological and distributional data, strong-ly support the existence of a previously

TABLE 2

Factor Loadings of Principal Component Analysisfor Selected Cranial Measurements Available from

the Slightly Damaged Holotype of Emballonuraatrata and Compared to Specimens from All

Four OTUsa

Variable Factor 1 Factor 2

Mastoid width 0.855 20.329

Rostral width 0.853 0.128

Greatest zygomatic breadth 0.834 20.356

Interorbital width 0.662 0.708

Eigenvalue 2.58 0.752

% total variance 64.7 18.8

a The number of variables used is reduced because of

the state of the holotype.


undescribed species in the dry areas ofnorthern and western Madagascar.

DISCUSSION

NOTES ON NATURAL HISTORY

Emballonura tiavato is a delicately flying batthat is among the first species to becomeairborne at dusk. They have been captured atAnkarana and other sites in the dry north onseveral occasions actively foraging in theforest understory when the last fading raysof daylight still remain. The stomach contentsof one individual of E. tiavato collected inthe Daraina area in November 2001 contain-ed the wing scale remains of a Lepidoptera(Razakarivony et al., 2005).

All of the individuals of Emballonura wehave captured on Madagascar were obtainedat the entrance of caves and rock overhangs or

in areas with rock outcrops, and on the basisof this field experience, this genus is notsynanthropic. However, Peterson et al.(1995) reported that near the eastern humidforest site of Perinet [5 Andasibe], a localinhabitant brought to them a specimen thathad been obtained in a house. We assume thatthis individual was actively feeding and simplysought shelter between foraging bouts ratherthan using the house as a day-roost. A largenumber of dwellings and buildings in villageswithin the eastern humid forest zone havebeen surveyed for synanthropic-living speciesof bats and no sign of Emballonura has beenfound (F. H. Ratrimomanarivo, personalcommun.). In May 2005 at Marovaza, up tofive individuals of E. tiavato were found afterdusk roosting on the ceiling of a housewithout windows and within 5 m of anexposed limestone tsingy rock face. Theseanimals did not use the house as a day-roost,

Fig. 6. Projection of factor 1 and factor 2 in principal component analysis of select cranial measurementsof the holotype of Emballonura atrata and specimens from the four OTUs. The oval to the right is associatedwith specimens we allocate to E. atrata and includes the holotype of that species and specimens from theeastern humid forest (OTU 2). The circle to the left encompasses the specimens allocated to E. tiavato fromthe drier regions of the island (OTUs 1, 3, and 4). Loading contributions of variables to each axis are shownin table 2.


Fig. 7. Unrooted network analysis of Malagasy Emballonura spp. D-loop sequences. Each labeled circlerepresents a unique haplotype; unlabeled circles represent missing inferred haplotypes. Numbers by the linesconnecting haplotypes indicate the number of mutational steps at each connection. The thick line indicatesthe division between species.


Fig. 8. Unrooted network analysis of Malagasy Emballonura spp. cyt b sequences. Each labeled circlerepresents a unique haplotype; unlabeled circles represent missing inferred haplotypes. Numbers by the linesconnecting haplotypes indicate the number of mutational steps at each connection. The thick line indicatesthe division between species.


but rather as a resting site during nightforaging bouts.

On the basis of specimens we have exam-ined, we can offer the following insights aboutthe seasonality of reproduction in E. tiavato.On February 4, 2004, at Andavakoera, a fe-male was collected with a single embryo(crown-rump length of 16 mm), three otherfemales were obtained in full lactation, eachwith a single placental scar, and two weresubadults. Over the course of four days inmid-December 2004 in the region ofMarovaza and Anjajavy, a number of femaleswere captured that were pregnant and all withsingle embryos and large mammae. Theseincluded two individuals in a sea cave withembryo crown-rump lengths of 18 and 21 mm.Of six individuals captured at a slightly inlandcave, all were female, and five were carryingembryos (12–18 mm crown-rump length). Thesixth individual, an adult female, did not showany signs of reproductive activity. Given thatnot a single male was captured at this lattercave, it may have been the site of a nurserycolony. The only other pregnant female E.tiavato that we captured is an individual onNovember 5, 2001, in the Daraina area thathad a single embryo measuring 9 mm incrown-rump length. Females with enlargedmammae have been obtained in mid-April toearly May in Ankarana. We have not handleda male that was clearly in reproductivecondition, although one at Anjajavy onDecember 7, 2004, had testes measuring 3 32 mm and slightly convoluted epididymis,another at Andavakoera on February 4,2002, had 3 3 1 mm testes and slightlyconvoluted epididymis, and a third individualat Ankarana on May 19 had 4 3 2 mm testesand slightly convoluted epididymes. Thus, onthe basis of this information, we conclude thatthe litter size is one and it would appear thatthere is notable variation between populationsin northern and northwestern Madagascar asto the time of parturition. Evaluating whetherthis difference is associated with latitudinalvariation in seasonality or fluctuating fromyear to year based on local rainfall patternsrequires further field studies.

Much less information is available on thereproductive season of E. atrata. OnNovember 15, 2004, three females were

obtained near Midongy du Sud: One wasadult and showed no sign of sexual activityand the other two had enlarged mammae andsingle embryos (crown-rump length 15 mmand 18 mm). Russ and Bennett (1999) re-ported seeing a pair mating on a cave ceilingduring the month of March 1999 (J. Russ,personal commun.). Of three females collectedin late May 2005 near Kianjavato, two hadlarge mammae, no embryos, and one placentalscar each. The third individual was an adultwith no recent sign of breeding activity.

TAXONOMY, BIOGEOGRAPHY, AND CONSERVATION

Tate and Archbold (1939) identified a num-ber of cranial characters that they used toseparate species groups and species in thegenus Emballonura. They concluded that E.atrata had ‘‘simple’’ features assumed to beancestral character states for this genus (p. 5).Griffiths et al. (1991) reexamined and scoredthe character states identified by Tate andArchbold (1939) as apomorphic or plesio-morphic and used them in a cladistic analysis.Their results reflect those of Tate andArchbold (1939), indicating that E. atrata isthe least derived of any living Emballonuraand that it lacks a number of characters foundin other members of this genus. The characterstates scored by Griffiths et al. (1991) for E.atrata are identical to those found in E.tiavato. These include the presence of a nasalsulcus and absence of lateral rostral swelling,confluent basal pits, anterolateral extension ofthe basal (basisphenoid) pits, and posteriorrecession of basisphenoid pits. On the basis ofthese characters, E. atrata and E. tiavato forma species group and are each other’s closestrelatives, which implies a single colonizationof the island by this genus and subsequentspeciation.

Multiple species of Emballonura have beenfound to co-occur on several tropical islands.The highest species richness for any islandoccurs on New Guinea. Five species, includingMosia (often recognized as a subgenus ofEmballonura; Griffiths et al., 1991), occur inthe same general portion of the island and inmany cases in sympatry, and a sixth speciesoccurs on nearby islands (Flannery, 1995b;Bonaccorso, 1998). Thus, the presence of two


species of Emballonura on Madagascar is notexceptional, and current information indicatesthat they are allopatric in their distributions.

What is intriguing in a biogeographic senseis the complete absence of any species ofEmballonura on any other island in the IndianOcean. The westernmost non-Malagasy spe-cies is E. monticola, found in southernMyanmar, the Malay Peninsula, and theislands of Sumatra, Java, and Borneo(Simmons, 2005). There is a water expanse ofabout 5600 km between this species andMadagascar that crosses the islands or archi-pelagos of Andamar, Sri Lanka, Maldives,Seychelles, Mascarenes, and the Comoros.Island size probably does not explain theabsence of Emballonura from these differentsites, as members of this genus are knownfrom some very small western Pacific islands(Flannery, 1995b). Further, many of theseislands have caves and rock outcrops, the day-roost sites typically occupied by members ofthis genus. Finally, given the presumed abilityof Emballonura to reach Madagascar acrossa considerable expanse of water, its absencefrom the African continent is inexplicable.

Cornet (1974) devised a very useful systemto explain biotic variation on Madagascar inthe form of bioclimatic zones, very similar tothe life zone ecology of Holdridge (1964).Cornet’s system was based on data froma series of weather stations across the islandand calculated from the parameters of waterdeficit (annual rainfall minus potential evapo-transpiration), mean minimum temperaturein the coldest month of the year, and length ofthe dry season. Five different stages weredelimited in this system, and the wettestportion of the island fell under the ‘‘etagehumide’’ or moist stage. The line separatingthis stage from the four drier stages closelymatches the distributional limit of E. atrata(fig. 1). Further, the southern limit of E.tiavato, based on our survey data, alongthe western lowland portion of the islandcoincides with the division of ‘‘etage sec’’ ordry stage and ‘‘etage subaride’’ or subaridstage. There is a specimen record of Embal-lonura from Toliara (Peterson et al., 1995: 57),but we have not captured a member of thisgenus during several bat inventories in theregion.

Emballonura tiavato occurs across the drierportions of Madagascar, including the north-ern and western lowland portions of theisland. This species seems to be broadlydistributed in karstic limestone areas of thelowland central west, particularly in the regionnorth of Mahajanga. It is known to occur inseveral protected areas including the ReserveSpeciale d’Ankarana, Reserve Specialed’Analamerana, and Parc National deBemaraha (Goodman et al., 2005), as well asfrom numerous sites outside of the existingreserve system.

Fewer precise details are available on thedistribution of E. atrata in the east, ascompared to E. tiavato in the west. In theMNHN there is a series of close to 25specimens of E. atrata collected in theMaroantsetra area over the course of 2 weeksin the mid-1930s. A label in one jar with 19specimens (1947-289a to 1947-289t) reads,‘‘Brought in by natives who said that theyhad removed them from small caves orcrevices in rocks in forest.’’ On the MasoalaPeninsula, not far from Maroantsetra, a cavecolony was found with at least 100 bats,a portion of which were E. atrata, and in thissame region up to three individuals have beenfound together in hollow standing anddowned tree trunks (Russ and Bennett,1999). During a mid-November 2003 surveyof the Parc National de Midongy du Sud andsurrounding region a group of about 10individuals was located in an undergroundrock shelter with a small hole opening to thesurface (S. M. Goodman, unpubl.). Thisspecies appears to be broadly distributedacross lowland areas of the complete lengthof the eastern humid forest, a region nearly1500 km in length, but has not been reportedfrom many protected areas. However, feweastern lowland reserves have been surveyedfor bats.

Emballonura spp. on Madagascar are notcollected as wild meat, presumably because oftheir small size and because they are notknown to form large colonies. Members ofthis genus tend to live in day-roosts associatedwith forest habitat and they may be among thefew bat species on the island that are forestdependent (Goodman et al., 2005). In ourexperience, it is highly unusual to capture


Emballonura out of forest settings. Thus, themaintenance of natural habitat may be im-portant for their long-term survival. Further,a variety of different types of human use ofcaves might disturb day-roosting individualsand pose another potential threat to theEmballonura.

ACKNOWLEDGMENTS

It is with pleasure that we acknowledge theassistance of the Association Nationale pourle Gestion des Aires Protegees (ANGAP) andthe Direction des Eaux et Forets for issuingpermits to conduct this research. The aid oftwo different colleagues, Daniel Rakoton-dravony and Olga Ramilijaona, in their rolesas departmental chairs of the Departement deBiologie Animale, Universite d’Antananarivo,in certain administrative details is greatlyappreciated. A portion of our bat surveyfieldwork was undertaken with the financialaid of Bat Conservation International, theEllen T. Smith and Marshall Field funds ofthe Field Museum of Natural History, theNational Geographic Society (6637-99 and7402-03), The National Speleological Society,and the Volkswagen Foundation, under theprotocol of collaboration between the Uni-versite d’Antananarivo, WWF-Madagascar,and Field Museum of Natural History. Thisresearch was partially based upon worksupported under a National Science Foun-dation Graduate Research Fellowship (toSGC). We are indebted to the followingcurators for access to specimens in their care(museum acronyms defined above inMaterials and Methods section): Rob Voss(AMNH), Michel Trainer and Jean-MarcPons (MNHN), Chris Smeenks (RMNH),Judith Eger (ROM), Daniel Rakotondravony(UADBA), Michael Carleton and LindaGordon (USNM), Rainer Hutterer (ZMAK),and Robert Asher (ZMB). For hospitality andlogistic aid we are grateful to Marc LeGroumellec and Rao Manavendra ofUNIMA and Philippe Girard, ThierryRanarivelo, and Abel Nirina at Marovaza.Several colleagues helped in the fieldwork andthese include Achille Raselimanana, FanjaRatrimomanarivo, Mamy Ravokatra, andVola Razakarivony. We also kindly acknowl-

edge Richard Jenkins and his associates of BatConservation Madagascar for allowing usaccess to specimens collected by this researchgroup. We are indebted to Harald Schutz andJohn Weinstein for providing photographs,Lucienne Wilme for the map, and RebeccaKramer for line drawings. Paula Jenkinshelped with an important bibliographic detail.Robert Voss and two anonymous reviewersprovided helpful comments on an earlierversion of this paper.

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APPENDIX 1

SPECIMENS OF EMBALLONURA SPP. FROM MADAGASCAR USED IN THIS STUDY

Abbreviations used: PN 5 Parc National, RS 5 Reserve Speciale

Emballonura tiavato—Province d’Antsiranana:Ambanja, lower Sambirano River (MCZ 45087–88); Andavaka Matsaborimadio, at edge ofMatsaborimadio, 10.5 km NE Ambondromifehy,12u48.6259S, 49u15.2529E, 290 m (FMNH 179239);Andavadrano, 5.5 km SE Ambery, 12u50.6329S,49u20.8979E, 330 m (FMNH 179238); Foretd’Andavakoera, Grotte d’Andakaty, 2.9 km NBetsiaka, 13u07.7789S, 49u14.0399E, 210 m(FMNH 179357–364); Foret de Binara, 7.5 kmSW Daraina, 13u159180S, 49u369590E (FMNH172680); Nosy Be, Pointe a la Fievre (MNHN1985.410); RS d’Analamerana, Grotte de Bazaribe,3.6 km SE de Menagisy, 12u42.7289S, 49u28.4119E,90 m (FMNH 178800–802); RS d’Ankarana,2.6 km E Andrafiabe, near Andrafiabe Cave,12u55.99S, 49u03.49E, 50 m (FMNH 169705,176275–276, 176360–361); RS d’Ankarana,Antsironandoha Cave (west), 10 km NWMahamasina, 12u539200S, 49u59510E, 100 m(FMNH 173002); RS d’Ankarana, AmbahibeCave, 2 km W Mahamasina, 12u589030S, 49u79130,100 m (FMNH 173003); RS d’Ankarana, Grotted’Ambahibe, 3.0 km NW Mahamasina, 12u58950S,49u079090E, 80 m (FMNH 176270–274). Provincede Mahajanga. Marovaza, 14u56948.00S,47u16928.60E, 5 m (FMNH 184025-026); 4.0 kmNE Anjajavy, 14u59.7139S, 47u13.9169E, 10 m(FMNH 184080); 3.0 km NE Anjajavy,15u0.4719S, 47u14.3319E, 10 m (FMNH 184018–024); 18.5 km S. Anjajavy, 15u11.4269S,

47u12.1759E, 50 m (FMNH 184016–017); 26.5 kmSW Anjajavy, 15u11.8719S, 47u02.5349E, sea level(FMNH 184013-015); PN de Bemaraha,Anjohitantely, 19u08.4609S, 44u48.7839E, 64 m(UADBA uncataloged RBJ 157, 158, 162).

Emballonura atrata—Province de Fianarantsoa.Fort Carnot [5 Ikongo] (MCZ 45649); grotte au Nde Vondrozo (MCZ 45089); Kianjavato,21u22.4429S, 47u51.6049E, 150 m (FMNH 185224–226); W slope of Mt. Ambatobe, 1.2 km ENEAmpatramary, 9.5 km NE Midongy su Sud,23u30.69S, 47u03.19E, 650 m (FMNH 178677,178595–596). Province de Toamasina: Hiaraka,Baie d’Antongil, Masoala (MNHN 1985.948);Maroantsetra (MNHN 1985.411); 20 km SWMaroantsetra (FMNH 74198–74203; MNHN1947.288 [7 specimens], 1947.289 A a T [19 speci-mens], 1996.358–360); 40 km NW Maroantsetra(MNHN 1947.288 [7 specimens]); Perinet [5Andasibe] (MNHN 1985.418, ROM 42056); regiond’Antanambe, Mananara (MNHN 1997–2133);Rogez (MNHN 1984.757–758); Tamatave [5Toamasina] (MCZ 16401–402). Province deToliara. Evondro [5 Isaka-Ivondro?], valley ofhigh Fanjahira (MCZ 45081–086); MarovonyForest, 24u089S, 47u229E, 30 m (USNM 577062–063). Uncertain localities. Aus dem Innern vonMadagaskar (holotype, ZMB 4692); Grande foretde l’Est (MCZ 45091); probably cote est (MCZ57538); Tanala (MCZ 45647).


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al

com

pari

son

so

fm

easu

rem

ents

of

E.

tia

vato

an

dE

.a

tra

taw

ere

con

du

cted

toex

am

ine

dif

fere

nce

sb

etw

een

the

sex

es:

*P

,0

.05

,*

*P

,0

.01

,*

**P

,0

.00

1.

Des

crip

tiv

est

ati

stic

so

fex

tern

al

mea

sure

men

tsp

rese

nte

din

bo

ldw

ere

ma

de

by

the

sam

efi

eld

coll

ecto

r(S

MG

).T

oex

am

ine

dif

fere

nce

sin

exte

rna

lm

easu

rem

ents

ma

de

inth

efi

eld

,in

clu

din

gfo

rea

rm,

bet

wee

nth

ese

two

spec

ies

of

Em

ba

llo

nu

ra,

we

use

dth

eA

nk

ara

na

(OT

U1

)a

nd

Mid

on

gy

du

Su

d(s

ub

set

of

OT

U2

)sa

mp

les,

wh

ich

wer

em

easu

red

by

the

sam

efi

eld

coll

ecto

ra

nd

t-te

stst

ati

stic

al

com

pa

riso

ns

of

mea

sure

men

ts(s

exes

com

bin

edfo

rea

chsp

ecie

s),

wh

ile

tho

seo

fw

eig

ht,

dif

fere

nt

win

gb

on

es,

tib

ia,

an

dca

lca

rw

eu

sed

com

bin

edO

TU

s1

,3

,a

nd

4co

mp

are

dto

OT

U2

—in

bo

thca

ses

sex

esco

mb

ined

:+ P

,0

.05

,++

P,

0.0

1,

+++ P

,0

.00

1,

++++

P,

0.0

00

1.

To

tal

len

gth

Ta

ille

ng

thH

ind

foo

tle

ng

thE

ar

len

gth

Fo

rea

rmle

ng

thB

od

ym

ass

Em

ba

llon

ura

tia

vato

An

ka

ran

a(O

TU

1)

-5

7.5

63

.16

*1

5.7

61

.11

5.5

60

.53

12

.46

0.9

23

6.6

60

.74

3.1

60

.35

*

55

–64

,N

58

15

–18

,N

57

5–

6,

N5

51

1–

14

,N

58

36

–38

,N

58

2.7

–3.7

,N

58

U6

1.8

61

.30

16

.46

1.5

25

.86

0.4

51

2.8

60

.84

38

.26

2.3

93

.66

0.1

6

60

–63

,N

55

15

–18

,N

55

5–

6,

N5

51

2–

14

,N

55

35

–41

,N

55

3.4

–3.8

,N

55

sex

esco

mb

ined

59

.26

3.3

41

6.0

61

.28

5.6

60

.51

12

.56

0.8

83

7.2

61

.69

3.3

60

.40

55

–64

,N

51

31

5–

18

,N

51

25

–6

,N

51

31

1–

14

,N

51

33

5–

41

,N

51

32

.7–

3.8

,N

51

3

dry

reg

ion

site

s(O

TU

s1

,3

,4

)

-5

9.5

64

.25

**

*1

6.2

61

.26

5.8

60

.68

13

.16

1.0

43

7.6

61

.31

**

3.5

60

.52

**

55

–7

0,

N5

19

15

–18

,N

51

55

–7

,N

51

61

1–

15

,N

52

03

6–

41

,N

52

02

.7–

4.3

,N

52

0

U6

3.2

64

.02

17

.26

3.1

46

.06

0.5

01

3.2

61

.11

39

.06

1.5

64

.16

0.7

0

57

–70

,N

52

01

3–

24

,N

52

05

–7

,N

51

71

2–

15

,N

52

03

5–

42

,N

52

13

.0–

6.0

,N

52

0

sex

esco

mb

ined

61

.46

4.4

81

6.8

62

.50

5.9

60

.60

13

.26

1.1

53

8.3

61

.60

3.6

60

.54

+++

55

–70

,N

53

91

3–

24

,N

53

65

–7

,N

53

31

1–

16

,N

54

13

5–

42

,N

54

22

.7–

4.5

,N

53

7a

Em

ba

llon

ura

atr

ata

ho

loty

pe

(ZM

B4

69

2)

——

5.8

—3

9.4

—

Mid

on

gy

du

Su

d

U6

5.0

63

.46

+1

8.7

61

.15

++6

.06

0.0

01

6.3

62

.31

+++

40

.36

0.5

8++

5.9

61

.10

63

–69

,N

53

18

–20

,N

53

6–

6,

N5

31

5–

19

,N

53

40

–41

,N

53

5.0

–7.1

,N

53

east

coa

st(O

TU

2)

U6

3.2

63

.71

18

.46

1.7

76

.06

0.4

81

4.9

61

.89

39

.66

1.2

55

.36

0.9

3++

++

58

–69

,N

54

16

–21

,N

58

5–

7,

N5

10

13

–19

,N

58

37

–42

,N

51

35

.0–

7.1

,N

56

AP

PE

ND

IX2

EX

TE

RN

AL

ME

AS

UR

EM

EN

TS

(in

mm

)A

ND

BO

DY

MA

SS

(in

g)

OF

EM

BA

LL

ON

UR

AT

IAV

AT

OA

ND

E.

AT

RA

TA


To

tal

len

gth

Tail

len

gth

Hin

dfo

ot

len

gth

Ear

len

gth

Fo

rea

rmle

ng

thB

od

ym

ass

sex

esco

mb

ined

62

.36

4.1

11

7.8

62

.09

6.5

60

.92

14

.66

1.6

23

8.8

61

.36

5.3

60

.93

57

–67

,N

57

14

–21

,N

51

15

–8

,N

51

51

3–

19

,N

51

23

7–

42

,N

55

05

.0–

7.1

,N

56

E.

bec

carr

i6

0.7

62

.00

12

.06

1.1

58

.06

0.0

01

5.9

61

.07

58

–6

3,

N5

71

0–

13

,N

57

8–

8,

N5

71

4–

17

,N

57

37

.5–

42

.0,

N5

54

1b

3.5

–5

.0,

N5

37

b

E.

raff

ray

an

a

-b

—1

0.5

–1

2.7

,N

51

0—

11

.0–1

3.1

,N

51

03

7.5

–4

1.8

,N

51

45

.0–

6.0

,N

51

4

Ub

—1

1.7

–1

4.0

,N

54

7.0

–8

.5,

N5

41

1.5

–1

5.2

,N

54

38

.7–4

1.6

,N

57

4.2

–6

.0,

N5

3

3rd

dig

it3

rdd

igit

4th

dig

it4

thd

igit

met

aca

rpa

l1

stp

ha

lan

xm

eta

carp

al

1st

ph

ala

nx

tib

iaca

lca

r

Em

ba

llon

ura

tia

vato

An

ka

ran

a

-3

1.0

61

.12

14

.26

0.5

72

3.5

60

.90

8.9

60

.31

14

.66

1.1

71

4.5

61

.06

30

.1–

32

.5,

N5

41

3.7

–1

5.0

,N

54

22

.7–2

4.7

,N

54

8.4

–9

.1,

N5

41

3.1

–1

6.1

,N

56

13

.6–

16

.4,

N5

6

U3

1.0

61

.04

13

.96

0.5

52

4.0

61

.09

9.0

60

.52

15

.36

0.2

51

5.0

60

.41

29

.9–

32

.7,

N5

51

3.5

–1

4.9

,N

55

22

.8–2

5.3

,N

55

8.4

–9

.6,

N5

51

4.9

–1

5.5

,N

55

14

.5–

15

.6,

N5

5

sex

esco

mb

ined

31

.06

1.0

11

4.0

60

.54

23

.86

1.0

08

.96

0.4

21

4.9

60

.92

14

.76

0.8

5

29

.9–

32

.7,

N5

91

3.5

–1

5.0

,N

59

22

.7–2

5.3

,N

59

8.4

–9

.6,

N5

91

3.1

–1

6.2

,N

51

11

3.6

–1

6.4

,N

51

1

dry

reg

ion

site

s

-3

1.5

61

.11

14

.36

0.6

02

4.1

61

.12

*8

.76

0.3

0*

15

.26

0.8

61

4.0

60

.87

*

29

.8–

33

.1,

N5

16

12

.9–

15

.0,

N5

16

22

.7–

26

.0,

N5

16

8.1

–9.3

,N

51

61

3.1

–1

6.2

,N

51

81

2.9

–1

6.4

,N

51

8

U3

2.2

61

.10

14

.46

0.5

02

4.8

61

.00

9.0

60

.45

15

.56

0.6

61

4.4

60

.68

29

.9–

34

.0,

N5

20

13

.7–

15

.3,

N5

20

22

.8–

26

.3,

N5

20

8.2

–9

.8,

N5

20

13

.9–1

6.7

,N

52

01

3.3

–1

5.6

,N

52

0

AP

PE

ND

IX2

(Co

nti

nu

ed)


To

tal

len

gth

Tail

len

gth

Hin

dfo

ot

len

gth

Ea

rle

ng

thF

ore

arm

len

gth

Bo

dy

ma

ss

sex

esco

mb

ined

31

.96

1.1

5+

14

.36

0.5

3++

24

.56

1.1

18

.96

0.4

2++

15

.46

0.7

71

4.2

60

.84

+++

29

.8–3

4.0

,N

53

71

2.9

–1

5.3

,N

53

72

2.7

–2

6.3

,N

53

78

.1–

9.8

,N

53

71

3.1

–1

6.7

,N

53

91

2.3

–1

6.4

,N

53

9

Em

ba

llon

ura

atr

ata

ho

loty

pe

(ZM

B4

69

2)

34

.2—

15

.3—

26

.6—

Mid

on

gy

du

Su

d

U3

3.6

–3

4.0

,N

52

15

.1–

15

.5,

N5

2+

25

.5–2

6.9

,N

52

9.0

–10

.0,

N5

21

5.8

–1

6.3

,N

52

15

.1–

15

.7,

N5

2

east

coa

st(O

TU

2)

-3

3.0

61

.26

14

.46

0.8

72

5.2

61

.18

15

.06

0.1

7*

*

31

.8–

34

.3,

N5

31

3.9

–1

5.4

,N

53

24

.5–2

6.6

,N

53

8.7

–9.3

,N

52

14

.9–1

5.2

,N

53

15

.3,

N5

1

U3

2.7

61

.51

15

.06

0.5

82

5.3

61

.14

9.3

60

.39

16

.16

0.6

51

5.9

60

.60

29

.0–

35

.3,

N5

15

13

.6–

16

.1,

N5

15

22

.7–2

7.1

,N

51

58

.8–

10

.1,

N5

15

15

.4–1

7.5

,N

51

31

4.8

–1

6.9

,N

51

3

sex

esco

mb

ined

32

.76

1.2

61

4.8

60

.59

25

.26

0.9

69

.26

0.3

61

5.8

60

.72

15

.76

0.6

3

29

.0–

35

.3,

N5

26

13

.6–

16

.1,

N5

26

22

.7–2

7.1

,N

52

58

.7–

10

.1,

N5

24

14

.8–1

7.5

,N

52

41

4.8

–1

6.9

,N

52

1

aD

oes

no

tin

clu

de

pre

gn

an

tfe

ma

les

wit

hm

od

era

teto

larg

eem

bry

os.

bB

ase

do

nm

easu

rem

ents

pre

sen

ted

inB

on

acc

ors

o(1

99

8)

an

dh

ind

foo

tin

clu

des

the

cla

w.

AP

PE

ND

IX2

(Co

nti

nu

ed)


Des

crip

tiv

est

ati

stic

sp

rese

nte

da

sm

ean

6st

an

da

rdd

evia

tio

n(m

inim

um

2m

ax

imu

m,

N).

Sep

ara

tet-

test

sta

tist

ica

lco

mp

ari

son

so

fm

easu

rem

ents

of

E.

tia

vato

an

dE

.a

tra

taw

ere

con

du

cted

toex

am

ine

dif

fere

nce

sb

etw

een

the

sex

es:

*P

,0

.05

.T

oex

am

ine

dif

fere

nce

sin

cra

nia

la

nd

den

tal

mea

sure

men

tsb

etw

een

thes

etw

osp

ecie

so

fE

mb

all

on

ura

,w

eu

sed

OT

Us

1,

3,

an

d4

com

pa

red

toO

TU

2a

nd

t-te

stst

ati

stic

al

com

pa

riso

ns

of

mea

sure

men

ts(s

exes

com

bin

edfo

rea

chsp

ecie

s):

+ P,

0.0

5,

++P

,0

.01

,++

+ P,

0.0

01

,++

++P

,0

.00

01

.

Gre

ate

stsk

ull

len

gth

toca

nin

es

Gre

ate

stzy

go

ma

tic

bre

ad

thIn

tero

rbit

al

wid

thM

ast

oid

wid

thB

rain

case

hei

gh

tR

ost

ral

wid

th

Em

ba

llo

nu

rati

ava

to

An

ka

ran

a(O

TU

1)

-1

2.7

60

.31

7.4

60

.10

2.4

60

.11

6.7

60

.24

6.1

60

.15

5.3

60

.20

12

.2–1

3.0

,N

57

7.2

–7

.5,

N5

72

.3–

2.6

,N

57

6.4

–7.0

,N

57

5.9

–6.3

,N

56

5.1

–5.6

,N

57

U1

2.8

60

.25

7.5

60

.13

2.4

60

.05

6.8

60

.10

6.1

60

.13

5.4

60

.06

12

.5–1

3.1

,N

54

7.3

–7

.6,

N5

42

.3–

2.4

,N

55

6.7

–6.9

,N

55

6.0

–6.3

,N

55

5.3

–5.4

,N

54

sex

esco

mb

ined

12

.76

0.2

87

.46

0.1

22

.46

0.0

96

.76

0.2

06

.16

0.1

45

.36

0.1

6

12

.2–1

3.1

,N

51

17

.2–

7.6

,N

51

12

.3–

2.6

,N

51

26

.4–

7.0

,N

51

25

.9–

6.3

,N

51

15

.1–

5.6

,N

51

1

dry

reg

ion

site

s(O

TU

s1

,3

,4

)

-1

3.0

60

.40

7.4

60

.18

*2

.66

0.1

56

.86

0.1

86

.26

0.1

85

.56

0.1

8

12

.2–1

3.6

,N

51

97

.0–

7.7

,N

51

82

.3–

2.8

,N

51

96

.4–

7.0

,N

51

95

.8–

6.4

,N

51

75

.1–

5.7

,N

51

9

U1

3.0

60

.32

7.6

60

.15

2.5

60

.11

6.9

60

.14

6.1

60

.20

5.5

60

.10

12

.5–1

3.5

,N

52

07

.3–

7.8

,N

51

92

.3–

2.7

,N

52

16

.7–

7.2

,N

52

15

.9–

6.5

,N

51

95

.3–

5.7

,N

52

0

sex

esco

mb

ined

13

.06

0.3

6++

7.5

60

.17

+++

2.5

60

.14

+++

6.8

60

.17

++++

6.2

60

.19

+++

5.5

60

.14

++++

12

.2–1

3.6

,N

54

07

.0–

7.8

,N

53

82

.3–

2.8

,N

54

16

.4–

7.2

,N

54

15

.8–

6.5

,N

53

75

.1–

5.7

,N

54

0

Em

ba

llo

nu

raa

tra

ta

ho

loty

pe

(ZM

B4

69

2)

13

.27

.82

.77

.06

.56

.0

Mid

on

gy

du

Su

d

U7

.86

0.1

02

.76

0.2

07

.26

0.1

76

.46

0.2

66

.06

0.1

5

13

.4–1

3.5

,N

52

7.7

–7

.9,

N5

32

.5–

2.9

,N

53

7.1

–7.4

,N

53

6.1

–6.6

,N

53

5.9

–6.2

,N

53

east

coa

st(O

TU

2)

-1

3.4

60

.12

7.8

60

.36

2.7

60

.07

7.1

60

.10

6.5

60

.35

5.7

60

.08

13

.3–1

3.5

,N

53

7.5

–8

.2,

N5

32

.6–

2.8

,N

55

7.0

–7.2

,N

53

6.1

–6.8

,N

53

5.6

–5.8

,N

54

U1

3.3

60

.34

7.8

60

.27

2.6

60

.15

7.1

60

.20

6.4

60

.15

5.8

60

.28

12

.8–1

3.8

,N

58

7.4

–8

.4,

N5

12

2.4

–2.9

,N

51

26

.7–

7.4

,N

51

26

.1–

6.6

,N

51

15

.3–

6.2

,N

51

1

AP

PE

ND

IX3

CR

AN

IAL

AN

DD

EN

TA

LM

EA

SU

RE

ME

NT

S(i

nm

m)

OF

EM

BA

LL

ON

UR

AT

IAV

AT

OA

ND

E.

AT

RA

TA


Gre

ate

stsk

ull

len

gth

toca

nin

es

Gre

ate

stzy

go

ma

tic

bre

ad

thIn

tero

rbit

al

wid

thM

ast

oid

wid

thB

rain

case

hei

gh

tR

ost

ral

wid

th

sex

esco

mb

ined

13

.36

0.2

97

.86

0.2

72

.76

0.1

37

.26

0.1

76

.46

0.1

95

.86

0.2

3

12

.8–

13

.8,

N5

13

7.4

–8.4

,N

51

52

.4–

2.9

,N

52

06

.7–

7.4

,N

51

86

.1–

6.8

,N

51

45

.3–

6.2

,N

51

6

C1–

C1

M3–

M3

C1–

M3

Em

ba

llon

ura

tia

vato

An

ka

ran

a

-3

.36

0.1

55

.56

0.1

44

.86

0.1

0

3.1

–3

.5,

N5

75

.4–

5.7

,N

57

4.7

–5

.0,

N5

7

U3

.36

0.0

65

.56

0.0

84

.86

0.0

9

3.2

–3

.3,

N5

45

.4–

5.6

,N

54

4.7

–4

.9,

N5

5

sex

esco

mb

ined

3.3

60

.12

5.5

60

.11

4.8

60

.09

3.1

–3

.5,

N5

11

5.4

–5.7

,N

51

14

.7–

5.0

,N

51

2

Dry

reg

ion

site

s

-3

.36

0.1

35

.56

0.1

44

.96

0.1

3

3.1

–3

.5,

N5

19

5.3

–5.8

,N

51

94

.7–

5.2

,N

51

9

U3

.36

0.0

95

.66

0.1

35

.06

0.1

2

3.2

–3

.5,

N5

20

5.4

–5.9

,N

52

04

.7–

5.2

,N

52

1

sex

esco

mb

ined

3.3

60

.11

5.6

60

.13

++4

.96

0.1

3++

++

3.1

–3

.5,

N5

40

5.3

–5.9

,N

54

04

.7–

5.2

,N

54

1

Em

ba

llon

ura

atr

ata

Ho

loty

pe

(ZM

B4

69

2)

3.5

5.7

5.2

Mid

on

gy

du

Su

d

U3

.3–

3.5

,N

52

5.7

–6.0

,N

52

5.1

–5

.2,

N5

2

east

coa

st

-3

.46

0.2

05

.86

0.3

25

.26

0.1

3

3.2

–3

.6,

N5

35

.4–

6.0

,N

53

5.0

–5

.3,

N5

4

U3

.36

0.2

65

.86

0.2

15

.16

0.1

0

3.0

–3

.7,

N5

11

5.4

–6.0

,N

51

24

.9–

5.2

,N

51

2

sex

esco

mb

ined

3.3

60

.23

5.7

60

.21

5.1

60

.10

3.0

–3

.7,

N5

17

5.4

–6.0

,N

51

94

.9–

5.3

,N

52

0

AP

PE

ND

IX3

(Co

nti

nu

ed)


A New Species of Emballonura (Chiroptera - Yoder Lab

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