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AMERICAN MUSEUMNovitatesPUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORYCENTRAL PARK WEST AT 79TH STREET, NEW YORK, N.Y. 10024

Number 2742, pp. 1-45, figs. 1-33, table 1 August 2, 1982

Systematics of the New World Nectar-Feeding Bats(Mammalia, Phyllostomidae), Based on the

Morphology of the Hyoid and Lingual Regions

THOMAS ALAN GRIFFITHS'

ABSTRACT

Dissection and histological examination of thehyoid and lingual regions of the New World nec-tar-feeding bats reveal marked modification ofthetongue retractor musculature (Mm. sternohyoi-deus, geniohyoideus, hyoglossus, styloglossus, andgenioglossus) and modification of the internal andexternal tongue structure from the conditionsfound in non-nectar-feeding bats. Use of thesederived characters in a cladistic analysis leads tothe phylogenetic hypothesis that nectivory evolvedtwice independently in the family Phyllostomidae.One group of nectar-feeding phyllostomids, com-prising the genera Lonchophylla, Lionycteris, andPlatalina (traditionally considered glossopha-gines) deserves separate subfamilial status basedon the markedly different adaptations for necti-

vory observed. The other group, comprising theremaining 10 glossophagine genera (Glossopha-ginae, sensu stricto), plus Phyllonycteris, Ero-phylla, and perhaps Brachyphylla form a mono-phyletic group. Within the newly restrictedsubfamily Glossophaginae there are two majorclades. One clade is composed of Glossophaga,Monophyllus, and surprisingly, Lichonycteris. Theother is composed of the more derived nectar-feeding genera: Leptonycteris, Anoura, Hylonyc-teris, Choeroniscus, Choeronycteris, and probablyScleronycteris and Musonycteris. Interestingly,both karyotypic evidence, and evidence from den-tal and basicranial studies, can be interpreted tosupport the phylogeny presented here.

INTRODUCTIONFor almost 15 years the systematic status

of the New World nectar-feeding bats(subfamily Glossophaginae) has been dis-puted. Baker (1967) first suggested that thesubfamily Glossophaginae might not be amonophyletic group on the basis ofhis karyo-typic studies of several genera of the group.Since then Baker and others (see Baker, 1970,

1973; Baker and Lopez, 1970; Gerber andLeone, 1971; Phillips, 1971; Stock, 1975;Gardner, 1977; Baker and Bass, 1979; Bakeret al., 1981) have continued to examine thisquestion, but while many investigators agreethat the group is probably not monophyletic,there is little agreement as to exactly how thegroup should be properly divided.

' Assistant Professor of Biology, Illinois Wesleyan University, Bloomington, IL 61701.

Copyright © American Museum of Natural History 1982 ISSN 0003-0082 / Price $3.20

AMERICAN MUSEUM NOVITATES

In addition to the comparatively largesubfamily Glossophaginae, there is a smallergroup of endemic Antillean genera that areat least partly nectivorous. These genera havebeen traditionally placed in a separatesubfamily, the Brachyphyllinae (=Phyllo-nycterinae, Miller, 1907). However, recentkaryological work (Baker and Bass, 1979) andimmunological work (Baker et al., 1981) in-dicated that the Brachyphyllinae may beclosely related to Glossophaga and Mono-phyllus (both glossophagines). This findingled Baker and Bass (1979) to question thevalidity of the subfamily Brachyphyllinae,and to once again suggest that the Glosso-phaginae might not be a monophyletic group.The hyoid and lingual regions of the glos-

sophagine bats are highly modified (Sprague,1943; Wille, 1954; Winkelmann, 1971;Greenbaum and Phillips, 1974; Howell andHodgkin, 1976; Griffiths, 1978a) presumablyto permit the hyperextension of the tonguerequired for nectar-feeding. These modifi-cations are complex and extensive, and thusare ideal for use as derived characters (apo-morphies, Hennig, 1966) in a cladistic study.The main purpose of this paper is to attemptto resolve the question of the monophyly ofthe subfamily Glossophaginae via dissectionof the hyoid region and histological exami-nation of the tongue. Secondary purposesinclude resolving the exact systematic rela-tionship of the three genera of the othernectar-feeding subfamily (Brachyphyllinae)to the Glossophaginae, and determining therelationships of the genera within eachsubfamily to one another. To accomplishthese goals, representative species of eachgenus of glossophagine (except Musonycterisand Scleronycteris, which were unavailable)were dissected and compared with represen-tative species ofeach genus ofbrachyphyllinebat, and with a variety of species ofnon-nec-tar-feeding phyllostomid bats.

HISTORY OF THE PROBLEMThe first attempt at a unified classification

of a large number of New World bats wasthat of Dobson (1878). Dobson recognizedtwo subfamilies within the family Phyllo-stomidae: the Lobostominae (=Mormoopi-dae, Smith, 1972) and the Phyllostominae.

Within the Phyllostominae, he recognizedfour "groups": the Vampyri, the Glossopha-gae, the Stenodermata, and the Desmo-dontes. The Glossophagae contained 10species in seven genera. These genera wereGlossophaga, Phyllonycteris, Monophyllus,Ischnoglossus (=Leptonycteris), Loncho-glossa (=Anoura), Glossonycteris (=Anoura),and Choeronycteris.The "group" Glossophagae was considered

distinct from all other phyllostomids on thebasis of: (1) the long, narrow muzzle; (2) thelong, extensible tongue "clothed with filiformpapillae"; and (3) the deep groove in thelower lip. Except for the inclusion of Phyl-lonycteris, today considered to be groupedwith Brachyphylla and Erophylla in a sepa-rate, endemic Antillean subfamily, the"group" Glossophagae includes all the batsthen known that are today considered to be-long to the subfamily Glossophaginae.

Miller (1907) reexamined the speciesknown to Dobson, plus specimens in theUnited States National Museum and mu-seums in Paris, Leiden, and Berlin. Basinghis classification on the structure ofthe wing,sternum, shoulder girdle, and tooth cusps,Miller divided the Chiroptera into two sub-orders, 17 families, and 19 subfamilies. Allsubsequent classifications of the Chiropteraare based on Miller's work, including Simp-son (1945), Hall and Kelson (1959), Koop-man and Cockrum (1967), Koopman andJones (1970), Smith (1976), and Hall (1981).Miller (1907) divided the family Phyllostom-idae into seven subfamilies: the Chilonycter-inae (=family Mormoopidae, Smith, 1972),Phyllostominae, Stenoderminae, Phyllonyc-terinae (=Brachyphyllinae, Baker, 1979),Hemiderminae, Sturnirinae, and Glosso-phaginae. Miller (1907) recognized that Phyl-lonycteris, "Reithronycteris" (=Phyllonyc-teris, Koopman, 1952), and Erophylladeserved separate subfamilial status on thebasis of the "peculiar" tooth structure andthe modified noseleaf. Miller also added thegenera Lonchophylla, Hylonycteris, and Li-chonycteris to the subfamily Glossophaginae,and recognized Dobson's "Ischnoglossa" and"Glossonycteris" as Leptonycteris and An-oura, respectively. With the addition of fivemore genera (Scleronycteris, Thomas, 1912;

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GRIFFITHS: NECTAR-FEEDING BATS

Lionycteris, Thomas, 1913; Choeroniscus,Thomas, 1928; Platalina, Thomas, 1928;and Musonycteris, Schaldach and Mc-Laughlin, 1960), the subfamily Glossophag-inae was generically complete as it is tradi-tionally recognized today.However, recent investigations in the areas

ofchromosome morphology, immunologicalreactions ofblood sera, and hard morphologyof the basicranial skull and teeth have givenrise to speculation that the classic "Glosso-phaginae" may not be a monophyletic group.Baker (1967, 1970), on the basis of chro-mosome morphology, suggested that Lepto-nycteris sanborni, Glossophaga soricina, G.alticola, and G. commissarisi form a distinctgroup which may be more closely related toPhyllostomus hastatus, Macrotus water-housii, and Trachops cirrhosus (all subfamilyPhyllostominae) than to two other glossoph-agines: Choeronycteris mexicana and Choe-roniscus godmani. Baker (1967) hypothe-sized that the Glossophaginae may actuallybe an artificial grouping of nectar-feeders,evolved from two or more independent lines.Choeronycteris and Choeroniscus karyotypi-cally showed great similarity to Carollia sub-rufa and Carollia perspicillata (subfamilyCarolliinae), whereas another glossophagine,Anoura geoffroyi, showed similarities to boththe Leptonycteris-Glossophaga group and theChoeronycteris-Choeroniscus group, but waskaryotypically distinct from each. Baker andLopez (1970) added Monophyllus redmanito the Leptonycteris-Glossophaga group. Theyalso, however, examined the karyotypes ofbats of the other New World nectar-feedingsubfamily, the Brachyphyllinae (=Phyllo-nycterinae) and found that the chromosomesofErophylla and Brachyphylla (both brachy-phyllines according to Silva Taboada andPine, 1969; and Nagorsen and Peterson,1975) are similar to each other, and to thoseof the Leptonycteris-Glossophaga-Mono-phyllus group. Further work by Baker (1973),Gardner (1977), and Baker and Bass (1979),confirmed this finding, and both Gardner(1977) and Baker and Bass (1979) suggestedthat the Brachyphyllinae (=Phyllonycteri-nae) be grouped with the Glossophaga-Mono-phyllus group within the Glossophaginae (seefig. 1).Gerber and Leone (1971), studying the

immunologic reactions of sera of glossoph-agine bats, also suggested that the Glosso-phaginae were an artificial grouping ofnectar-feeders. They too suggested that there was adistinct Glossophaga group and a distinctChoeronycteris group. However, relation-ships of these groups to non-glossophagineswere directly opposite to those suggested byBaker (1967). Glossophaga soricina andGlossophaga commissarisi were immunolog-ically more closely related to Carollia thanto Choeronycteris; Choeronycteris mexicanawas most closely related to Phyllostomus,Chrotopterus (both phyllostomines), and sur-prisingly, to Desmodus, the vampire bat.Recent electrophoretic and albumin immu-nological work by Baker et al. (1981) seemto contradict the karyotypic studies further.Baker et al. (1981) presented evidence thatAnoura, Glossophaga, Monophyllus, Lepto-nycteris, Hylonycteris, and Choeroniscus forma clade. This suggestion directly contradictsthe karyotypic studies (see Baker, 1967;Baker and Bass, 1979) that suggest the Glos-sophaginae are not monophyletic.

Stock (1975) contributed to the Baker/Ger-ber and Leone controversy by reexaminingchromosomes of Carollia and Choeroniscususing G and C banding techniques. Stockshowed that although the gross chromosomalmorphology of Carollia and Choeroniscus issimilar, banding patterns show that there isno relationship between Carollia and Choe-roniscus [refuting half of Baker's (1967) hy-pothesis].

Slaughter (1970) examined dentitions of anumber of bats, including a few glossopha-gines. Although he did not divide the Glos-sophaginae into two formal groups, Slaughterdid observe that "primitive" glossophaginessuch as Glossophaga and phyllostominessuch as Macrotus may have shared a recentcommon ancestor. Slaughter (1970) alsonoted the similarity between "advanced"glossophagine (Choeroniscus-type) teeth, andthe teeth of carolliines and desmodontines(vampires). Phillips (1971) examined thedentitions of the glossophagines, although ina much more rigorous manner. Phillips alsosplit the Glossophaginae into two groups (seefig. 2). In regard to the origins of these twogroups, he suggested that the teeth of Choe-ronycteris resemble those of Phyllostomus,

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FIG. 1. Relationships among the genera of the Glossophaginae. Redrawn from Gardner (1977).

Mimon, Chrotopterus (all phyllostomines),and Carollia (Carolliinae), whereas the teethof Glossophaga and Leptonycteris resemblethose of Macrotus and Artibeus (a phyllo-stomine and a stenodermatine).There are a number of other, less rigorous

works that have made reference either to theorigin (or origins) of the Glossophaginae, orto the possibility of a polyphyletic, falsegrouping of the nectar-feeders into a singlesubfamily. Walton (1967), on the basis ofpostcranial osteology, suggested that the glos-sophagines arose as a group from a Vampy-rops-like stenodermatine ancestor. Waltondid not suggest a polyphyletic origin for theGlossophaginae, although he did mentionthat Glossophaga-like bats resemble steno-dermatines much more than do Choero-nycteris-like bats. Interestingly, Walton (1967)believed that the Brachyphyllinae arose froma primitive Macrotus-like ancestor. Walton,in suggesting that the relationship betweenthe brachyphyllines and glossophagines is notclose, was at variance with the proposals of

Baker (1967), Baker and Bass (1979), andGardner (1977) to include the brachyphyl-lines with Glossophaga, Monophyllus, andLeptonycteris.Other workers have also supported a

schism within the Glossophaginae, althoughthey have not always suggested that the glos-sophagines are a polyphyletic group. Forman,Baker and Gerber (1968), Forman (1971) onthe stomach morphology of bats, and Wille(1954) on glossophagine tongues, observedbasic morphological differences betweenGlossophaga-like and Choeroniscus-likeglossophagines. Forman, Baker and Gerbertentatively suggested that there was a rela-tionship between Choeronycteris and severalnon-glossophagines (Chrotopterus, Phyllo-stomus, and Desmodus).Only two works deal comprehensively with

the relationships within the subfamily Glos-sophaginae. These are the work of Phillips(1971) on tooth and basicranial morphology,and the work by Gardner (1977) on karyol-ogy. Both papers divide the Glossophaginae

4 NO. 2742


IE -ChoeronycterisMusonycterisChoeroniscus-Platalina*Lichonycteris-Hylonycteri s-Scleronycteris. Lionycteris-Loncho ph yl la*Anoura-LeptonycterisGlossophagaMonophyl lus

FIG. 2. Relationships among the genera of the Glossophaginae. Redrawn from Phillips (1971).

into essentially the same discrete groups (seefigs. 1 and 2), but in the proposed relationshipof these groups to one another, these twopapers differ considerably. Phillips (197 1)divided the Glossophaginae into two majorgroups: (1) a group containing Choeroniscus,Choeronycteris, and Musonycteris which hecalled the "Choeronycteris-group"; and (2) alarge group containing the remaining 10 glos-sophagine genera which he called the "Glos-sophaga-group." On the basis of molar con-figurations, he then divided the latter groupinto three subgroups: (1) Glossophaga,Monophyllus, and Leptonycteris; (2) Loncho-phylla, Lionycteris, and Anoura; and (3) Scle-ronycteris, Lichonycteris, Hylonycteris, andPlatalina. Of these three subgroups, the An-oura subgroup was considered most primi-tive, or most like the hypothetical glos-sophagine ancestor that Phillips proposed.The Platalina subgroup was considered mostderived.Gardner (1977) generally followed Phillips

(1971) in his breakdown of the Glossophag-inae into subgroups (see fig. 1). There weretwo basic differences. First, Anoura wasplaced in its own group, separate from otherglossophagines. This placement reflectedGardner's belief that Anoura has had a sep-arate evolutionary history from the other

genera of glossophagines. Second, and ofgreat interest, Platalina, Lichonycteris, Hy-lonycteris, Scleronycteris, Lionycteris, andLonchophylla were placed with the Choero-nycteris-group, whereas Phillips (197 1) placedthese bats with the Glossophaga-group. Bothresearchers agreed that the subfamily Glos-sophaginae might not be monophyletic. It isof further interest that Gardner (1977) ten-tatively placed the Brachyphyllinae with theglossophagine genera Leptonycteris, Glos-sophaga, and Monophyllus in his phylogeny.If the Glossophaginae are monophyletic,however, Gardner (1977) concluded that allmodern glossophagine karyotypes could havebeen derived from a primitive karyotypesimilar to the present day Lonchophylla tho-masi karyotype.The use of the hyoid and lingual regions:

It is obvious from the preceding discussionthat there are differences of opinion on thephylogeny of the Glossophaginae. Much ofthe confusion has resulted from lack of rec-ognition of the fact that it is incorrect to useshared primitive characters (symplesio-morphies) to unite taxonomic groups. Withfew exceptions (e.g., Baker and Bass, 1979),no effort has been made to differentiate de-rived from primitive character states. Un-fortunately, the few studies that have done

I

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so have been hampered by a lack of suitablespecimens ofsome ofthe rarer glossophaginegenera.

Previous work on the hyoid region of bats(Sprague, 1943; Wille, 1954; Winkelmann,1971; and Griffiths, 1978a, 1978b) demon-strated that the hyoid muscles controlling thetongue are markedly modified in the Glos-sophaginae, apparently to permit the tongueto be extended and manipulated for nectar-feeding. Work on the tongue structure ofthe Leptonycteris-Glossophaga-Monophyl-lus group (Wille, 1954; Winkelmann, 1971;Greenbaum and Phillips, 1974; Howell andHodgkin, 1976; and Griffiths, 1978a) and theChoeronycteris group (Wille, 1954; Winkel-mann, 1971) has demonstrated that intrinsicand extrinsic tongue structure is distinctlydifferent in the two groups ofglossophagines,and that in both groups these structures arevery different from those of non-glossopha-gine bats. Until the current study, however,the majority of the genera of glossophagineshad not been examined.

Modifications for nectar-feeding are somarked (Griffiths, 1978a) that they appearto be irreversible without abandoning thenectar-feeding niche. Stated another way, allmodifications for nectar-feeding are clearlyapomorphies, and thus ideal for use in a taxo-nomic study. The sole problem, then, is todetermine which are true shared, derivedcharacters (synapomorphies, and useful intaxonomy) and which are convergent char-acters (misleading unless recognized as such).Specialized mechanisms for tongue hyper-extension have evolved independently in theMammalia several times (Doran and Baggett,1971), and although the overall mechanismin every known case is similar, there are ob-servable morphological differences amongthem. Thus the question of the monophylyof the taxon Glossophaginae should be re-solvable by observations of the hyoid andlingual regions to answer the question: did amorphology facilitating nectar-feeding evolvemore than once in the phyllostomid bats?

MATERIALS AND METHODS

Fluid preserved specimens ofthe followingspecies were dissected (species are listed herein the traditional taxonomic classification for

ease to the reader, but see the SystematicConclusions for my arrangement):

Family PhyllostomidaeSubfamily "Glossophaginae"

Glossophaga soricina: Texas Tech Uni-versity (TTU) Nos. 3326, 3327, 3328,3329, 3330. All from Mexico, Ta-maulipas, La Gruta de Quintero. Uni-versity of Michigan Museum of Zo-ology (UMMZ) 11 1278, 111280,111294,111300,111301,111302.Allfrom Costa Rica, Cartago, 1 mi. S Car-tago, Agua Caliente.

Monophyllus redmani: University ofMassachusetts (UMA) 2252, 2258.Both from Haiti, Dept. du Sud, Reyn-olds Station above Miragoane, 2000ft.

Leptonycteris sanborni:UMMZ 122935,122936,122937,122938,122939. Allfrom Arizona, Cochise Co., 9 mi. SWSan Simon.

Lichonycteris obscura: National Mu-seum ofNatural History, SmithsonianInstitution (NMNH) 519892. FromPanama, Darien, Tacarcuna Village,1900 ft. NMNH 432194. Collectionlocality unknown.

Anoura geoffroyi: UMMZ 108640,108641, 108653, 108655, 108680,108681. All from Chiapas, 1 mi. STuxtla Gutierrez.

Hylonycteris underwoodi: AmericanMuseum ofNatural History (AMNH)238199. From Panama, Darien, CerroMali, 1400 m. NMNH 506578. FromCosta Rica, Heredia Prov., Finca LaSalva, Rio Puerto Viejo.

Choeroniscus godmani: NMNH 522934.From Venezuela, Yaracuy, San Felipe,Puente Marroquina.

Choeronycteris mexicana: UMMZ77750, 77751. From Mexico, Sonora,Pilares. UMMZ 77755, 77756. FromMexico, Sonora, El Tigre Mtns.UMMZ 77760. From Mexico, So-nora, St. Marie Mtns.

Lonchophylla robusta: UMMZ 114923,114927, 114928, 114929, 114930,114933. All from Costa Rica, Limon,Los Diamantes, 4 mi. N Headquar-ters, 250 m.

6 NO. 2742


Lionycteris spurrelli: NMNH 499771.Colombia, Antioquia, Zaragoza.

Platalina genovensium: NMNH 268766.Peru, Carivelli.

SUBFAMILY Brachyphyllinae (=Phyllonyc-terinae)Brachyphylla cavernarum: Personal col-

lection, T. Griffiths (TAG) 2, andUMA 3086. Both from Puerto Rico.

Erophylla sezekorni: AMNH 164255,164281. From Bahamas, New Provi-dence, Hunt's Cave.

Phyllonycteris poeyi: AMNH 176023.From Cuba, Habana, 3 mi. E Tapaste,Cueva del Indio. TAG 1, 3. Haiti?

Subfamily PhyllostominaeMacrotus waterhousii: TTU 12484,

12485,12486, 12487, 12488. All fromArizona, Pinal Co., 25 mi. S CasaGrande-Old Mammon Mine. Univer-sity of Vermont (UVM) 2372, 2374.From Haiti, Dept. du Sud, 1 mi. SEDuchity, 2400'. UVM 2939, 2410.Haiti, Dept. du Sud. AMNH 120972,120977. From Dominican Rep., Cha-von, E of La Romana, caves near theriver.

Phyllostomus hastatus: AMNH 202308.Trinidad.

Micronycteris nicefori:UMA 2819. FromPanama.

Subfamily StenodermatinaeArtibeusjamaicensis: UVM 1651, 1656.From Haiti, Dept. du Sud. UVM3501, 3503. From Haiti, Dept. duSud, 6 km. SW Miragoane, 580 m.

Phyllops haitiensis: UVM 2750. Haiti,Dept. du Sud.

Uroderma bilobatum: UMA 3034. Pan-ama, Colon Prov., Santa Rosa.

Vampyressa pusilla: UMA 3334. Pan-ama Canal Zone, Bohio Point Ridge.

Vampyrops helleri: UMA 2695. Trini-dad, St. George Co., Simla, 5 mi. NArima.

Subfamily CarolliinaeCarollia perspicillata: UMA 3060. Pan-ama Canal Zone, 2 km. N Frijoles.

Subfamily DesmodontinaeDesmodus rotundus: AMNH 208895,

208899, 208902. All from Mexico,Oaxaca, S Felipe del Agua (Cerro S.Felipe).

Additionally, the basicranial region andteeth of the following specimens were ex-amined:

Glossophaga soricina: AMNH 92234,92235, 92236, 92237, 92238, 92239,92240, 92241, 92242, 92631, 92700.

G. longirostris: AMNH 130665.Monophyllus redmani: AMNH 19106,

19107, 23782, 23783, 41157.Lichonycteris obscura: NMNH 331258,

335187, 362595, 364348, 483374.Leptonycteris nivalis: NMNH 88017,

88018, 88019, 88026.Leptonycteris curasoae: NMNH 101850,

105130 (alcoholic with skull re-moved), 434424.

Anoura geoffroyi: NMNH 88022, 88023,92260, 92263, 92420, 319248,319250, 319251, 323182.

Anoura caudifer: NMNH 483371,499308, 499309, 499310.

Hylonycteris underwoodi: NMNH331260, 337984.

Scleronycteris ega: NMNH 407889.Lonchophylla thomasi: AMNH 209358.NMNH 361570, 361571, 393013,460097.

Lonchophylla hesperia:NMNH 498827,498828, 498829, 498830, 498831.

Lonchophylla handleyi: NMNH 507172.Lionycteris spurrelli: AMNH 97220,

97221, 97222, 97224, 97260, 97261,97264. NMNH 499303, 499304,499305, 499306.

Platalina genovensium: NMNH 268765(alcoholic with skull removed).

Because of small size, muscles of manyspecimens were exceedingly fragile. Forma-lin-preserved specimens were less prone tomuscle breakage than those specimens whichhad been stored in isopropyl alcohol for along period. A binocular dissecting micro-scope was used for all dissections. Completedrawings ofall dissections and other anatom-ical preparations were made at a scale ofeither lOX or 5X the natural size. From these,selected drawings showing specific anatomi-cal differences were inked for presentation.Tongue sectioning for all species examined

followed classic histological technique as de-scribed in Humason (1972). Tongues wereexcised just anterior to the hyoid bone (ba-

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sihyal), as close to the bone as possible. Eachtongue was then re-fixed in buffered formalinsolution, embedded in paraffin, and sec-tioned. Staining was done with Mallory Tri-ple Connective Tissue Stain, and/or with he-matoxylin and eosin. All measurementsgiven to identify particular tongue segmentsare in microns from the tip of the tongue.

In the descriptive sections of this paper,the morphology of Glossophaga soricina isdescribed in great detail. All other glos-sophagines, and then all other bats dissectedare described in less detail in separate sec-tions under each muscle. At the end of eachmuscle description is a section entitled"Comments." This section is designed to em-phasize the functional and systematic high-lights of each muscle, points to be especiallyremembered when reading the SystematicConclusions.

ACKNOWLEDGMENTSThis work was part ofthe author's doctoral

dissertation at the Univeristy of Massachu-setts. I am indebted to the members of mydoctoral committee, Drs. David Klingener,Margery Coombs, Karl Koopman, CharlesPitrat, Dana Snyder, and Donald Kroodsma,for their thoughtful guidance during thecourse ofthis study and for their careful read-ing of the manuscript. I am grateful to Dr.James Dale Smith for his rigorous review ofthe manuscript. I thank my fellow graduatestudents from the University of Massachu-setts Museum ofZoology for their friendshipand encouragement while this study was inprogress, particularly Jeanne Bertonis, Car-roll Schloyer, Doug Smith, and William Wall.I am grateful to my wife, Cara-Sue, and mydaughters Jennifer and Anne for their sup-port, and for putting up with me during thetough moments of preparing this work.

I thank the following individuals and in-stitutions for providing me with specimens:Dr. Karl F. Koopman, American Museumof Natural History; Dr. Charles 0. Handley,National Museum ofNatural History, Smith-sonian Institution; Dr. Robert J. Baker, TheMuseum, Texas Tech University; Dr. PhilipMyers, University of Michigan Museum ofZoology; Dr. David J. Klingener, University

of Massachusetts Museum of Zoology; andDr. Charles A. Woods, University of Ver-mont Museum of Zoology.This work was supported in part by Uni-

versity Fellowship #87015 from the Uni-versity of Massachusetts. Illinois WesleyanUniversity generously provided logisticalsupport in the preparation ofthe manuscript,plus technical support from Pat Meyers andthe Media Center in mounting the illustra-tions. Special thanks to Judith Switzer forassistance.

Finally, I will always be grateful to the lateDr. Herbert Potswald for his friendship, sup-port, and interest in my work.

DESCRIPTION OF THE MUSCLESBRANCHIOMERIC MUSCULATURE

MYLOHYOID GROUP

The muscles of this group are innervatedby the mylohyoid nerve, a branch ofN. man-dibularis, which is a branch of N. trigeminus(V). The mandibular nerve enters both ofthemuscles described on their deep surfaces.

M. MYLOHYOIDEUSFigures 3, 6, 9, 11, 14, 16, 18

ORIGIN: In Glossophaga soricina, from themedial surface of the mandible. The originextends for much of the length of the man-dibular ramus, from a point about 1 mm.posterior to the symphysis to the angle ofthejaw.

INSERTION: Into its antimere, forming araphe along the ventral midline of the jawregion.OTHER GLOSSOPHAGINES: The muscle is the

same in all glossophagines dissected. In someindividuals, the mylohyoid is quite thin an-teriorly, to the point of revealing the genio-hyoid beneath. This anterior thinness is vari-able within a species; however, in all casesthe mylohyoid consists of a solid sheet ofmuscle.OTHER BATS: In the three genera of brach-

yphyllines, the origin and insertion of themylohyoid are the same, but there is a slightbreak in the muscle anteriorly. This has theeffect of dividing the mylohyoid into thick

8 NO. 2742


M.

M.

-'--M. masseter sup.

M. digastricus

M. styloglossusM. mand.-hby.

M. omohyoideus M. hyoglossus

M. sternomastoideuss- XX M. sternohyoideus

FIG. 3. Ventral view of the superficial hyoid musculature of Glossophaga soricina. Bar = 1 mm.

anterior and posterior parts, separated by afleshy aponeurosis. In all three phyllosto-mines, there is a pronounced break, whichresults in the mylohyoid having a distinctanterior and a distinct posterior part. This isalso the case in all five stenodermatine generadissected. In Carollia and Desmodus, themylohyoid is a single sheet. This is particu-larly true in Carollia; the specimen I dis-

sected had the most robust mylohyoid mus-cle I have ever observed on a bat.COMMENTS: Obviously, there are two quite

different conditions for this muscle in thePhyllostomidae: (1) a single, non-dividedmylohyoid found in all glossophagines, Ca-rollia, and Desmodus; and (2) a divided my-lohyoid found in all phyllostomines andstenodermatines. In the Brachyphyllinae,

1 982 9


-M. genioglossus

S4-M. styloglossus

I/M. digastricus

M. geniohyoideus,deep insertion

- M. sternomastoid.

FIG. 4. Ventral view of the deep hyoid musculature of Glossophaga soricina. Bar = 1 mm.

there is an aponeurosis anteriorly where themuscle becomes quite thin, but the muscleis essentially unbroken as in the glossopha-

gines. The primitive condition is obviouslythe undivided one, found in most bats (seeSprague, 1943; Griffiths, 1978a, 1978b, and

M. I

M.

M.

M.

10 NO. 2742


M. geniohyoideus,deep insert.M. ceratohyoideus

M. styloglossus

auditory bulla .LV,fu

thyrohyal M.jugulohyoideusM. cricothyroideus M. stylopharyngeus

M. thyrohyoideustracheal_---- M. sternothyroideus

FIG. 5. Ventral view of the hyoid apparatus and larynx of Glossophaga soricina. Bar = 1 mm.

in press). The divided condition could verywell be a synapomorphy shared by the Phyl-lostominae and Sternodermatinae.

M. MANDIBULO-HYOIDEUSFigures 3, 4, 6, 7, 9, 10-12, 14, 16, 18, 19

M. mylohyoideus profundus (Griffiths, 1978a).

ORIGIN: In Glossophaga soricina, from themedial surface of the mandible, just dorsaland slightly posterior to the origin ofthe pos-terior edge of the mylohyoid.

INSERTION: This muscle passes deep to theanterior digastric and hyoglossus muscles, toinsert on the ventrolateral surface of the ba-sihyal bone, and into the lateral and dorsalfibers of the sternohyoid.OTHER GLOSSOPHAGINES: The muscle is the

same in all glossophagines dissected. In someindividuals, the insertion into the fibers ofthe sternohyoid is reduced or absent, but thisis variable within genera.OTHER BATS: This muscle is the same in

all bats dissected.COMMENTS: The mandibulo-hyoid muscle

obviously developed in the phyllostomidbats in response to the freeing of the ster-nohyoid-hyoglossus complex from the basi-hyal. Since the mylohyoid proper could no

longer directly act on the hyoid apparatus, itsfunction of lateral pull was assumed by thissmall muscle that I suggest may have origi-nally been part of the posterior mylohyoid.The mandibulo-hyoid is found in all phyl-lostomids, and thus is of no value for thetaxonomic problem at hand.

HYOID CONSTRICTOR GROUP

The muscles of this group are innervatedby branches of N. facialis (VII), some ofwhich are extremely small and difficult totrace completely.

M. STYLOHYOIDEUS

ORIGIN: In Glossophaga soricina, from themedial surface of the anterior '/2-1 mm. ofthe stylohyal bone. The origin of this muscleis very closely associated with the origin ofthe stylopharyngeus.

INSERTION: On the posterolateral tip of thethyrohyal and on the lateral basihyal.OTHER GLOSSOPHAGINES: This muscle is

similar in Monophyllus and Lichonycteris. InLeptonycteris this muscle is variable. Inabout half the specimens dissected it was ab-sent. In the other half, it was reduced to a fewfibers embedded in fascia. In Lonchophylla,

1 982 I1I


M. myl ohyoideus l A\

M. geniohyoideus-/ I -LlLM. genioglossus

M. omohyoid. M. styloglossusM. hyoglossus

M.mond.-hyoid.

M.digastricus

M. sternohyoideus

M. sternomastoid.

FIG. 6. Ventral view of the superficial hyoid musculature of Lonchophylla robusta. Bar = 1 mm.

Lionycteris, Platalina, Anoura, Hylonycteris,Choeroniscus, and Choeronycteris, this mus-cle was absent in all specimens dissected.

OTHER BATS: This muscle is present inPhyllonycteris and Erophylla, but completelyabsent in Brachyphylla. In Phyllonycteris,

12 NO. 2742


M. geniohyoideus L il---M. genioglossusM. styloglossus / N. hypoglossus

M.hyoglossus Il\\M. geniohyoideus,M.hyoglossus_ IXtdeep insertioM. digastricus M. mand.-hyoid.

M. sternomastoideus M. sternohyoideus

FIG. 7. Ventral view of the deep hyoid musculature of Lonchophylla robusta. Bar = 1 mm.

this is a well-defined muscle that originatesfrom the medial stylohyal and passes medi-ally and anteriorly to insert by tendon on thehyoid bone at the ceratohyal/epihyal joint.

In Erophylla this muscle is very reduced; itinserts on the ceratohyal only. In all phyllos-tomines and stenodermatines dissected, thismuscle is absent. The muscle is absent in

1982 13


Desmodus, but present (though reduced) inthe specimen of Carollia dissected. In Ca-rollia, the insertion is on the tip of the thy-rohyal.COMMENTS: Sprague (1943) reported that

this muscle was absent in most Microchirop-tera he dissected, including all phyllostomids.Obviously, the presence or absence of thismuscle is somewhat variable. Nevertheless,Phyllonycteris, Erophylla, Glossophaga,Monophyllus, Lichonycteris, Carollia andsome specimens of Leptonycteris share theplesiomorphic condition of retaining the sty-lohyoid. All other phyllostomids are apo-morphic in that they have lost the stylohyoid.

M. JUGULOHYOIDEUSFigures 5, 8, 13, 15, 17, 20

ORIGIN: In Glossophaga soricina, from thebasioccipital shelf, about 1 mm. posterior tothe auditory bulla.

INSERTION: This muscle passes ventrallyand anteriorly, curving around the posteriorsurface of the auditory bulla to insert on theexpanded lateral tip of the stylohyal bone.OTHER GLOSSOPHAGmIES: This muscle is

similar in Monophyllus, Lichonycteris, Lep-tonycteris, Anoura, Hylonycteris, Choeronis-cus, Choeronycteris, Lonchophylla, Lionyc-teris, and Platalina.OTHER BATS: This muscle is similar in all

phyllostomids dissected.COMMENTS: This muscle is comparatively

more robust in all "glossophagine" generadissected. Functionally, this is to be expected,because the jugulohyoid muscle must anchorthe distal end of the anterior hyoid comuagainst the pull of the styloglossus muscle(see M. styloglossus).

M. SPHINCTER COLLI PROFUNDUS

This muscle is nominally a skin muscle,but it is included here because it takes originfrom the basihyal region and is innervatedby N. facialis. Sprague (1943) also includedthis muscle in his work on the hyoid regionof bats.

ORIGIN: In Glossophaga soricina, this mus-cle originates from the fascia of the posteriormylohyoid region.

INSERTION: This muscle is extremely re-duced in all specimens examined, consisting

at most of a few fibers that pass laterally infascia, to insert weakly on the inner skin sur-face of the cervical region.OTHER GLoSSOPHAGMIES: This muscle is

similar in form in Monophyllus, Lichonyc-teris, Leptonycteris, Anoura. In Hylonycterisreduction is almost complete, and in Choe-roniscus and Choeronycteris no trace of thismuscle could be observed. In Lonchophylla,Lionycteris, and Platalina this muscle wasvery different in form. It consisted of twodistinct parts, both originating from the fas-cia of the posterior mylohyoid region as inGlossophaga. One part passed laterally to in-sert on the inner surface of the cervical skin.The other part passed anterolaterally to inserton the inner surface of the cervical skin at a45-degree angle just lateral to the mandible.OTHER BATS: In Brachyphylla, the sphinc-

ter colli profundus is very similar to the samemuscle in Lonchophylla. This muscle is ab-sent in Erophylla and Phyllonycteris, exceptfor fascial tracts that pass laterally where themuscle used to be. In the phyllostomines dis-sected, this muscle is quite variable. In Mi-cronycteris there are three distinct slips, alloriginating from the basihyal raphe region.One slip passes anterolaterally, one passeslaterally, and one passes posterolaterally.Macrotus and Phyllostomus both lack the slipthat passes posterolaterally, and thus haveonly two slips. All five genera of stenoder-matines have a sphincter colli profundus thatis similar: it consists of two bellies that passanteriorly, one anterior to the other. The an-terior slip is very similar to the anterior slipin the phyllostomines. The posterior slip issimilar to the slip in the phyllostomines thatpasses laterally, except that in the stenoder-matines it passes anteriorly as well as later-ally. In Carollia this muscle is similar to thecondition observed in Macrotus and Phyl-lostomus. In Desmodus, this muscle consistsonly ofa single slip that passes anterolaterallyfrom the basihyal region.COMMENTS: The plesiomorphic condition

is obviously having three distinct heads,passing anterolaterally, laterally, and pos-terolaterally (see Sprague, 1943). This isfound only in Micronycteris of all the batsdissected here. In Macrotus, Phyllostomus,all the stenodermatines, Carollia, Brachy-phylla, Lonchophylla, Lionycteris, and Pla-

14 NO. 2742


M. geniohyoideus, deep insert.

M. sternothyroideus

FIG. 8. Ventral view of the hyoid apparatus and larynx of Lonchophylla robusta. Bar = 1 mm.

talina the posterior slip of this muscle showsa progression ofloss, from only a single weaklateral slip to complete loss. In Erophylla andPhyllonycteris, this muscle is absent. Otherthan the distinctive "both bellies passing an-teriorly" found in all the Stenodermatinae,this muscle is so variable it seems to be ofminimal use in a systematic study. In theglossophagines, it is interesting that more"advanced" nectar-feeders have lost thismuscle, whereas Lonchophylla, Lionycteris,and Platalina have one ofthe more primitiveconditions observed. This argues against theplacement of these three genera with themore "advanced" glossophagines, as hasbeen done in the past (see Systematic Con-clusions).

GLOSSOPHARYNGEAL GROUP

The muscles of this group are innervatedby branches of N. glossopharyngeus (IX).

M. STYLOPHARYNGEUSFigures 5, 8, 13, 15, 17, 20

ORIGIN: In Glossophaga soricina, from theposteromedial border of the stylohyal bone,at a point about 2 mm. from the lateral tip.

INSERTION: This muscle passes medially toinsert in the fibers of the pharyngeal wall,

between the hyopharyngeus and thyropha-ryngeus muscles.OTHER GLOSSOPHAGINES: This muscle is


bats dissected.

M. CERATOHYOIDEUSFigures 5, 8, 13, 15, 17, 20

ORIGIN: In Glossophaga soricina, fromthe anterior edge ofthe thyrohyal bone (lesserhyoid cornu), and from the fibers of the thy-rohyoid muscle.

INSERTION: This muscle passes anteriorlyto insert on the medial tip of the stylohyal,on the epihyal, and on the lateral tip of theceratohyal bones.OTHER GLOSSOPHAGINES: This muscle is

similar in Monophyllus, Leptonycteris, andAnoura. In Lichonycteris, Hylonycteris,Choeroniscus, Choeronycteris, Loncho-phylla, Lionycteris, and Platalina it insertson the entire posterior surface of the epihyaland the lateral tip of the ceratohyal (not onthe medial stylohyal at all).OTHER BATS: In all three brachyphylline

1 982 15


M. mylohyoideus M. geniohyoideus

M. masseter suP.

M. mand.- hy.

M. stytoglossus

M. digastricus M. hyoglossus

M. sternomastoidGus M. sternohyoideus

FIG. 9. Ventral view of the superficial hyoid musculature of Choeronycteris mexicana. Bar = 1 mm.

genera, this muscle inserts on the ceratohyaland epihyal only. In the Phyllostominae andStenodermatinae the muscle insertion variesconsiderably among genera, with what ap-pears to be great taxonomic significance. InMicronycteris, the insertion is on the cera-

tohyal, epihyal, and medial stylohyal (as in

Glossophaga). In Macrotus and Phyllosto-mus, the insertion is only on the epihyal andstylohyal, with the reduced ceratohyal play-ing no part. In the Stenodermatinae, threedifferent conditions are seen. In Vampyressapusilla and Vampyrops helleri, insertion is onall three anterior cornu elements, as in Glos-

16 NO. 2742


M. genioglossus-

M. geniohyoideus

-' --M. masseter sup.

M. styloglossus M. mandibulo-hyoid.

M. geniohyoideus, deepM. digastricus insertion (cut)

M. hyoglossus

M. sternomastoideus M. sternohyoideus

FIG. 10. Ventral view of the deep hyoid musculature of Choeronycteris mexicana. Bar = 1 mm.

sophaga. In Artibeus and Phyllops, insertionis on the ceratohyal and epihyal only. In Uro-derma, insertion is on the ceratohyal and lat-eral basihyal. In Carollia, the insertion is asin Artibeus, and in Desmodus the insertionis as in Macrotus.COMMENTS: The plesiomorphic condition

is difficult to ascertain with certainty here dueto the wide variability of this muscle. It isinteresting to note that the three distinct con-ditions observed in the stenodermatines dis-sected correspond very well to the branchesofthe stenodermatine phyletic tree presentedby Baker (1973).

1 982 17


PHARYNGEAL CONSTRICTOR GROUP

The muscles of this group are innervatedby branches of the N. vagus (X) as follows:N. laryngeus cranialis innervates M. crico-thyroideus; N. recurrens innervates Mm. hy-opharyngeus, thyropharyngeus, and crico-pharyngeus.

M. CRICOTHYROIDEUSFigures 5, 8, 13, 15, 17, 20

ORIGIN: In Glossophaga soricina, from theentire ventral surface of the cricoid cartilage,medial to the origin of the cricopharyngeus.

INSERTION: This muscle passes anteriorlyand laterally fanning out to insert on the ven-tral and ventrolateral thyroid cartilage walls,and on the ventral edge ofthe short posteriorthyroid cornu.OTHER GLOSSOPHAGINES: This muscle is


bats dissected.COMMENTS: In all phyllostomids, this mus-

cle is very simple structurally (unlike mor-moopids and vespertilionids, see Griffiths,1978b, in press). This is associated, no doubt,with the diminished role played by echolo-cation in food gathering.

M. HYOPHARYNGEUS

M. constrictor pharyngeus superior, Sprague,1943; superior constrictor, Novick and Griffin,1961

This muscle is almost completely absentin Glossophaga soricina; only a few musclefibers of what may be the remnants of thismuscle were found attached to the dorsalbuccopharyngeal fascia. This is also the casein Monophyllus redmani, Lichonycteris ob-scura, Leptonycteris sanborni, Anoura geof-froyi, Hylonycteris underwoodi, Choeronis-cus godmani, Choeronycteris mexicana,Lonchophylla robusta, Lionycteris spurrelli,and Platalina genovensium.OTHER BATS: This muscle is similar (al-

most completely absent) in all brachyphyl-lines dissected, and in all other phyllostomidsdissected.

M. THYROPHARYNGEUS

M. constrictor pharyngeus medius, Sprague, 1943;middle constrictor, Novick and Griffin, 1961

ORIGIN: In Glossophaga soricina, from thedorsal surface ofthe tip ofthe thyrohyal bone(posterior hyoid cornu).

INSERTION: This muscle passes dorsally,then medially to. insert into the dorsal pha-ryngeal midline and into its antimere.OTHER GLOSSOPHAGINES: This muscle is

similar in all glossophagines dissected.OTHER BATS: This muscle is similar in all

bats dissected.

M. CRICOPHARYNGEUS

M. constrictor pharyngeus inferior, Sprague, 1943;inferior constrictor, Novick and Griffin, 1961

ORIGIN: In Glossophaga soricina, the mus-cle originates in several slips from the lateralborder of the cricoid cartilage and from theposterior thyroid cornu.

INSERTION: The posterior slips pass dor-sally to insert on the pharyngeal midline, andin their antimere. The anterior slips pass dor-sally and anteriorly to also insert on the pha-ryngeal midline and their antimeres.OTHER GLOSSOPHAGINES: This muscle is

similar in Monophyllus, Lichonycteris, Lep-tonycteris, Anoura, Hylonycteris, Choeronis-cus, and Choeronycteris. In Lonchophylla,Lionycteris, and Platalina there were onlytwo slips.OTHER BATS: In the Brachyphyllines the

muscle is similar, though there are only twoslips present. In all the phyllostomines andstenodermatines dissected, there are threeslips present in this muscle, as is the case inCarollia. In Desmodus, this muscle consistsof a single large slip.COMMENTS: Note that all "glossophagines"

except Lonchophylla, Lionycteris, and Pla-talina are similar.

MYOTOMIC MUSCULATURE

LINGUAL GROUP

The muscles of this group are innervatedby the N. hypoglossus (XII).

18 NO. 2742


M. mylohyoideuss

M. geniohyoideus

. styloglossusM. omohyoideus M. hyoglossus

M. digostricus. M. mand.-hyoid

M. sternom ostoid. M. sternohyoideus

FIG. 11. Ventral view of the superficial hyoid musculature of Brachyphylla cavernarum. Bar = 1 mm.

M. GENIOGLOSSUSFigures 4, 6, 7, 10, 12

ORIGIN: In Glossophaga soricina, from themedial surface of the anterior 1 mm. of themandible, deep to the origin of the genio-hyoid.

INSERTION: This muscle passes posteriorlyto insert into the ventral surface ofthe tonguejust lateral to the tongue midline. In G. sor-

icina this muscle curves laterally as it ap-proaches the basihyal bone. It inserts on theposterior 3 mm. of the venter of the tongue,and does not insert on the basihyal.OTHER GLoSSOPHAGINES: This muscle is

similar in Monophyllus, Lichonycteris, Lep-tonycteris, Anoura, Hylonycteris, Choeronis-cus, and Choeronycteris. In Lonchophyllaand Lionycteris this muscle begins inserting

1982 19


M. geniohyoideusN. hypoglossus_...M. mand.-hyoid..

M. styloglossusM. genioglossus-M. hyoglossus

LM. digastricus

M. sternomostoideus"" ) 'M. sternohyoideus

FIG. 12. Ventral view of the deep hyoid musculature of Brachyphylla cavernarum. Bar = 1 mm.

much farther anteriorly on the venter of thetongue. Instead of inserting in only the pos-terior 3 mm., this muscle inserts into the pos-terior half of the ventral tongue surface, justlateral to the midline. In Platalina, the ge-nioglossus inserts about halfway betweenthese two extremes, inserting into the pos-terior 7 mm. of the tongue.OTHER BATS: In the Brachyphyllinae, this

muscle inserts into much of the length of the

ventral tongue surface. It is interesting to notethat in all three brachyphyllines, this muscleseems to be in several parts, or slips, that areeasily separable. In all other phyllostomids,this muscle inserts over much of the ventraltongue surface.CoMMENTs: Once more, all the "glos-

sophagines" except Lonchophylla, Lionyc-teris, and Platalina are united by a synapo-morphous character. In this case, the

20 NO. 2742


basihyal M. ceratohyoideus

M. jugulohyoid.A. stylopharyngeussternothyroideus

FIG. 13. Ventral view of the hyoid apparatus and larynx of Brachyphylla cavernarum. Bar = 1 mm.

condition seen in Lonchophylla/Lionycteriscould be "ancestral" to the condition in theother glossophagines, or it could be indepen-dently derived. The genioglossus ofPlatalinais most easily derived from the Loncho-phylla/Lionycteris condition. There seems tobe an interesting synapomorphous conditionuniting the three brachyphyllines, too: theseparability of this muscle into slips.

M. HYOGLOSSUSFigures 3, 4, 6, 7, 9, 10-12, 14, 16, 18, 19

ORIGIN: In Glossophaga soricina, from theformer basihyal raphe (now disconnectedfrom the basihyal bone); or more accurately,from the insertion ofthe sternohyoideus. Thehyoglossus and sternohyoideus have fused toform a single muscle that passes unbrokenfrom the sternum to the tongue.

INSERTION: This muscle passes anteriorlyto insert in the posterior tongue surface, me-dial to the insertion of the styloglossus.OTHER GLOSSOPHAGINES: The hyoglossus

is similar in Monophyllus, Lichonycteris,Lonchophylla, Lionycteris, and Platalina. InLeptonycteris, Anoura, Hylonycteris, Choe-roniscus, and Choeronycteris the origin andinsertion are the same. The hyoglossi ofthese

bats, however, are covered completely by theexpanded insertion of the geniohyoideus,which forms a "tunnel" that encompasses thehyoglossus (see M. geniohyoideus). The ba-sihyal raphe has almost completely disap-peared, and the former break between thehyoglossi and sternohyoidei is not visible inany of these six genera, except as the pointat which the geniohyoideus inserts.OTHER BATS: In the Brachyphyllinae, this

muscle originates by tendon from the basi-hyal bone. In all other phyllostomids dis-sected, this muscle originates by a very shorttendon from the basihyal bone.COMMENTS: See M. geniohyoideus Com-

ments.

M. STYLOGLOSSUSFigures 3-20

ORIGIN: In Glossophaga soricina, from theexpanded distal tip ofthe stylohyal, and fromthe posterior 4 mm. of the lateral surface ofthe stylohyal bone.

INSERTION: This muscle passes anteriorlyand somewhat medially, to insert in the pos-terolateral "corner" of the tongue. The fibersof this muscle intermingle (at right angles)with those of the hyoglossus.OTHER GLOSSOPHAGINES: This muscle is

1982 21


M. omohyoldeus > 3 M. styloglossusN. hypoglossusM. hyoglossus

M. mand.-hyoid. M. digastricus

M. sternohyoidous

M. sternomostoideus

FIG. 14. Ventral view of the hyoid musculature of Phyllonycteris poeyi. Bar = 1 mm.

similar in Monophyllus, Lichonycteris, Lep-tonycteris, Anoura, Hylonycteris, Choeronis-cus, and Choeronycteris. In Lonchophylla,Lionycteris and Platalina the insertion ofthismuscle is not in the posterior "corner" of thetongue, but rather into the lateral tongue sur-face, as in the bats below.OTHER BATS: In the Brachyphyllinae, the

origin of this muscle is similar to that of theGlossophaginae. The insertion is into the lat-eral surface of the tongue for much of thetongue length. This is true of all phyllosto-mids dissected.COMMENTS: Occasionally, this muscle is

very reduced (LeptonycterisAMNH 122936),

or is composed of two distinct heads (Des-modus AMNH 208902). These seem to bepeculiarities of individual specimens, how-ever, and not entire species. The apomor-phous condition observed here (the posteriorinsertion of this muscle) is once again foundin all "glossophagines" other than Loncho-phylla, Lionycteris, and Platalina.

MEDIAL VENTRAL CERVICAL GROUP

The muscles of this group are innervatedby an anastomosis of nerves made up of theanterior cervical nerves, except for M. ge-niohyoideus which is apparently innervated

22 NO. 2742


M. stylopharyngeussternothyroideus

FIG. 15. Ventral view of the hyoid apparatus and larynx of Phyllonycteris poeyi.

by N. hypoglossus (XII). Despite the appar-ent differing innervations, these muscles aretreated as a group on the basis of similarembryonic differentiation (Edgeworth, 1916).

M. GENIOHYOIDEUSFigures 3-12, 14, 16, 18, 19

ORIGIN: In Glossophaga soricina, by ten-don from the medial surface of the mandibleat a point approximately 2 mm. lateral to thesymphysis.

INSERTION: There are actually two separateinsertions for this muscle: a superficial in-sertion and a deep insertion. As this musclepasses posteriorly, it splits. The superficialfibers pass ventral to the basihyal and con-tinue posteriorly to insert in the fibers of thehyoglossus, and in the fibers of the sterno-hyoideus via the former basihyal raphe. Thisinsertion is relatively weak. The deep fibersof this muscle insert directly on the anteriorsurface of the basihyal bone; this insertion isrelatively strong.OTHER GLOSSOPHAGINES: The geniohyoi-

deus is similar in Monophyllus, Lichonyc-teris, Lonchophylla, Lionycteris and Plata-lina. In Leptonycteris, Anoura, Hylonycteris,

Choeronycteris, and Choeroniscus the ge-niohyoideus is very different. The origin isessentially the same, though it is expandedlaterally on the medial mandible. The musclepasses posteriorly in the same fashion as inGlossophaga, and splits into a superficial anda deep insertion. The deep insertion is on theanterior face of the basihyal, as in Glos-sophaga. However, the superifical insertionis not relatively weak, as in Glossophaga.Rather it is very well developed and strong,inserting in a loop around the ventral anddorsal surfaces of the intersection of the hy-oglossus and sternohyoideus muscles. To dothis, the geniohyoideus literally forms a "tun-nel" around the hyoglossus, enclosing it al-most completely (see figs. 9 and 10).OTHER BATS: In the Brachyphyllinae, this

muscle inserts by tendon to the basihyal. Inall other phyllostomids, this muscle insertsvia short tendon to the basihyal.COMMENTS: There seem to be two apo-

morphous states in the glossophagine bats:(1) where the geniohyoid has a strong, deepbasihyal bone insertion, and a weak, super-ficial basihyal raphe insertion; and (2) wherethe geniohyoid has a strong insertion in bothplaces. In no. 2, the geniohyoid accomplishes

1982 23


.|.s.'jUIUIIyuIUeu5 tM. styloglossusM. omohyoideus M. hyoglossus

M. mand.-hyoid.

M. digas smn.hosidL

\\\a M. sternohyoideus

M. sternomostoid.

FIG. 16. The hyoid musculature of a phyllostomine bat, Macrotus waterhousii. Bar = 1 mm.

this strong insertion by forming a tunnelwhich envelops the hyoglossus. Conditionno. 2 could be derived from condition no. 1,or the two could have independently evolved.In any event, the tunnel insertion (conditionno. 2) is definitely an apomorphous conditionthat has never been reported for any othermammal group. It therefore most stronglylinks the genera that share this trait: Lepto-

nycteris, Anoura, Hylonycteris, Choero-niscus, and Choeronycteris.

M. STERNOHYOIDEUSFigures 3, 4, 6, 7, 9-12, 14, 16, 18

ORIGIN: In Glossophaga soricina, from thedorsal surface of the xiphoid process of thesternum.

24 NO. 2742


stylohyaolN

auditory bull

1. styloglossus

M. jugulohyoid.M. stylopharyngeus

sternothyroi deu s

FIG. 17. Ventral view ofthe hyoid apparatus and larynx ofa phyllostomine bat, Macrotus waterhousii.Bar = 1 mm.

INSERTION: This muscle passes anteriorlyto insert by raphe in the fibers ofthe hyoglos-sus and in the superficial fibers of the ge-niohyoideus muscle. There is no connectionto the hyoid apparatus.OTHER GLOSSOPHAGINES: The sternohyoi-

deus is similar in Monophyllus, Lichonyc-teris, Lonchophylla, Lionycteris, and Plata-lina. In Leptonycteris, Anoura, Hylonycteris,Choeroniscus, and Choeronycteris the originof the sternohyoid is similar to that in Glos-sophaga. The insertion is in the fibers of thehyoglossus, and in the highly modified cir-cular insertion of the geniohyoideus (see M.geniohyoideus). In one individual of Lon-chophylla robusta and Lionycteris spurrelliithere was a remnant of the basihyal tendonpresent.OTHER BATS: In the Brachyphyllinae, this

muscle originates from a point slightly pos-terior to the "normal" origin, although notshifted as far posteriorly as in the glos-sophagines. In Erophylla, medial fibers ofthis muscle originate from the anterior bodyofthe sternum (not the manubrium), whereasmore lateral fibers of this muscle originate

from the lateral manubrium and proximalhead ofthe clavicle. In Erophylla, the medialfibers alone have a shifted origin. In bothBrachyphylla and Phyllonycteris, the medialfibers take origin from the anterior body ofthe sternum as well, but also the more lateralfibers have a shifted origin too. They takeorigin from the proximal head ofthe first rib,instead of from the lateral manubrium. Inboth Brachyphylla and Phyllonycteris, thereare extremely weak, lateralmost fibers thatretain the origin from the medial head of theclavicle. In all three genera, the insertion ofthe sternohyoid is via tendon to the basihyalbone.

In all other phyllostomids except Desmo-dus, this muscle originates from the dorsalsurface of the manubrium of the sternum,and from the medial head of the clavicle andsterno-clavicular articulation. In Desmodus,the origin is similar to that of Phyllonycteris.COMMENTS: Obviously, the posterior shift

of the origin of the sternohyoid muscle is anapomorphous condition, as in the insertioninto the fibers of the hyoglossus, rather thanthe basihyal bone. All three brachyphyllines,

1982 25


. geniohyoideus-M. styloglossus

N. hypoglossus

M. sternohyoi

hyoideus

sternomastoideusFIG. 18. The superifical hyoid musculature of a stenodermatine bat, Vampyressa pusilla. Bar = I

mm.

including Brachyphylla, share a slightly pos-terad shifted origin of this muscle. Thequestion of whether the shifts in the glosso-phagines are synapomorphies or due to con-

vergence is discussed below.

M. STERNOTHYROIDEUSFigures 5, 8, 13, 15, 17

ORIGIN: In Glossophaga soricina, from thedorsal surface of the medial clavicle, just lat-eral to the sterno-clavicular articulation.

INSERTION: This muscle runs anteriorly toinsert on the lateral surface of the thyroidcartilage, just posterior to the origin of thethyrohyoideus muscle.OTHER GLOSSOPHAGINES: The sternothy-

roideus is similar in Monophyllus, Lich-onycteris, Leptonycteris, Anoura, Hylo-nycteris, Choeroniscus, Choeronycteris, Lon-chophylla, Lionycteris, and Platalina.OTHER BATS: The origin and insertion of

this muscle is the same in the Brachyphylli-nae and in all phyllostomids dissected.

M. OMOHYOIDEUSFigures 3, 6, 11, 14, 16

This muscle is reduced in all glossopha-gines and absent in many specimens.

ORIGIN: In Glossophaga soricina, from thedeep surface of the bone of the scapula im-mediately surrounding the scapular notch.

INSERTION: This muscle passes ventrallyand medially, curving around the cervicalarea deep to both the sternomastoid and clei-domastoid muscles. It inserts weakly in thefibers ofthe hyoglossus and mylohyoid mus-cles.OTHER GLOSSOPHAGINES: This muscle is

similar in Monophyllus (though slightly morerobust), Lichonycteris, Leptonycteris, Anoura(more reduced), Hylonycteris (more re-duced), Choeroniscus, and Choeronycteris

M.my

M.dii

26 NO. 2742


M. hyogilM. digasl

1. geniohyoldeus

M. thyrohyoid hyoideus

M. cricothyroideus

FIG. 19. The deep hyoid musculature of a stenodermatine bat, Vampyressa pusilla. Bar = 1 mm.

(extremely reduced). In Lonchophylla andPlatalina this muscle is much more robust.This muscle was not observed in the singlespecimen of Lionycteris dissected, but thiswas probably due more to the poor state ofpreservation of the hyoid region.OTHER BATS: In the Brachyphyllinae, the

origin and insertion of this muscle are intothe stemohyoid and mylohyoid muscles,though this muscle appeared to be absent inone specimen ofErophylla (AMNH 164281).In the remaining phyllostomids this musclewas variable within species. When present,the origin and insertion were the same as inBrachyphylla.COMMENTS: Because of the extreme vari-

ation observed, this muscle is unreliable asa taxonomic indicator.

M. THYROHYOIDEUSFigures 5, 8, 13, 15, 17

ORIGIN: In Glossophaga soricina, from thelateral surface of the thyroid cartilage, justanterior to the insertion of the sternothy-roideus muscle.

INSERTION: This muscle passes anteriorly,fanning out as it does so, to insert on thethyrohyal bone (posterior hyoid cornu) andpartially in the fibers of the ceratohyoideusmuscle.OTHER GLOSSOPHAGINES: The thyrohyoi-

deus is similar in all glossophagine bats dis-sected.OTHER BATS: The thyrohyoideus is similar

in all bats dissected.

TONGUE MORPHOLOGY ANDHISTOLOGY

EXTERNAL MORPHOLOGY

GLOSSOPHAGINAE: To avoid confusion andfacilitate comparison, I follow the terminol-ogy used by Greenbaum and Phillips (1974)in their work on the tongues of Leptonycterissanborni and L. nivalis. The tongues of all"glossophagines" except Lonchophylla,Lionycteris, and Platalina are similar (seefigs. 21, 27, 28, and 29). Greenbaum andPhillips (1974) identified seven types of pa-pillae on the tongues of Leptonycteris: hair-

1 982 27


M. ceratohyoideus ceratohyalM. stylopharyngeus epihyalM. styloglossus hyroh yl

bullaM. jugulohyoideus stylohyal

FIG. 20. Ventral view ofthe hyoid apparatus and larynx ofa stenodermatine bat, Vampyressa pusilla.Bar = 1 mm.

like papillae, horny papillae, bifid papillae,singly-pointed papillae (two types, fleshy andhooklike), fungiform papillae, and circum-vallate papillae. I agree completely with theclassification of papilla types as proposed byGreenbaum and Phillips (1974). See figure21 for relative placement of the various pa-pilla types on the tongue.The hairlike papillae are distributed over

the anterolateral surface of the tongue in all"glossophagines" except Lonchophylla,Lionycteris, and Platalina. These papillaeform an anterior "brush," presumed byGreenbaum and Phillips (1974) and Howelland Hodgkin (1976) to be used in nectar-feeding (see fig. 21). The horny papillae arefound in all "glossophagines" except Lon-chophylla, Lionycteris, and Platalina oneither side ofthe dorsal midline ofthe tongue.Their arrangement, shown in figure 22, is ofsome interest. Generally, they consist of twoor more large, posteriorly-directed papillae,surrounded by several smaller papillae. Theshape and number of horny papillae seemsconstant within a genus, but varies betweengenera except in the cases of Monophyllus!Glossophaga and Hylonycteris/Choeronis-cus/Choeronycteris. The bifid papillae, sin-gly-pointed papillae, and fungiform papillaeare distributed as shown in figure 21, and arecommon to all "glossophagines" except Lon-chophylla, Lionycteris, and Platalina (see be-

low). The circumvallate papillae are presentin all "glossophagines" except Lonchophylla,Lionycteris, and Platalina, where they areabsent. In Glossophaga, Monophyllus, Li-chonycteris, and usually Leptonycteris, thereare four circumvallate papillae: two lateraland two medial. In every specimen dissected,the lateral papillae were larger than the me-dial ones. In one specimen of Leptonycterissanborni, one medial circumvallate papillawas missing. In every specimen of Anoura,Hylonycteris, Choeroniscus, and Choeronyc-teris dissected only the two large lateral cir-cumvallate papillae were present.

In Lonchophylla, Lionycteris, and Plata-lina the external tongue morphology is com-pletely different. There are only two papillatypes present: short hairlike papillae andfleshy monofid papillae. Additionally, thereis a deep, longitudinal groove in the lateralsurface of the tongue from a point just pos-terior to the tip to the base ofthe tongue. Theshort hairlike papillae do not form a brushtip, but rather form a line just dorsal to andjust ventral to the longitudinal groove. Thefleshy monofid papillae coat the dorsaltongue surface. All other papilla types areabsent.BRACHYPHYLLINAE: The tongues of Ero-

phylla and Phyllonycteris are similar to oneanother, and to the tongues of the Glosso-phaga-type glossophagines. The tongue of

28 NO. 2742


LG

HLPHP

MCP

HP

H L P

FIG. 21. Upper left: the tongue of Macrotus waterhousii, dorsal surface. Upper right: the tongue ofLionycteris spurrelli, dorsal surface. Lower left: the tongue of Glossophaga soricina, dorsal surface. Lowerright: the tongue of Choeronycteris mexicana, dorsal surface. Bar = 1 mm. MCP = median circumvallatepapilla, LG = longitudinal groove, HP = horny papillae, HLP = hairlike papillae.

1982 29


oQ3o

A

E

B

°qUo0

F

C

00000000

G

°ooo

D

H

J

FIG. 22. The horny papillae of the bats examined in this paper. A. Brachyphylla, B. Phyllonycteris,C. Glossophaga, D. Monophyllus, E. Lichonycteris, F. Leptonycteris, G. Anoura, H. Hylonycteris, I.Choeroniscus, J. Choeronycteris. Bar = 1 mm.

Brachyphylla is morphologically different.The Brachyphylla tongue has horny papillae,singly-pointed papillae (mostly fleshy), fun-giform papillae, and circumvallate papillae.It does not have hairlike papillae at the tip,and no bifid papillae were observed. Figure23 shows the arrangement of papillae on thetongue of Brachyphylla. There are only twomedial (and no lateral) circumvallate papillaepresent.

In Erophylla and Phylionycteris, the tonguesare similar to that of Brachyphylla in somerespects, and to those ofthe Glossophaga-type"glossophagines" in others (see fig. 23). Nobifid papillae are present, but there are hair-like papillae forming a brush tip similar tothat of Glossophaga. Four circumvallate pa-pillae are present in all specimens dissected,though the medial two are always larger. Inall other respects, the tongues of Erophyllaand Phyllonycteris are similar to that ofBrachyphylla.

OTHER BATS: The three phyllostomine gen-era are similar. All three have horny papillae,singly-pointed (mostly fleshy monofid) pa-pillae, fungiform papillae, and circumvallatepapillae (two lateral and two medial). Figure21 shows the placement of these papillae onthe tongue surface. The horny papillae andthe circumvallate papillae are virtually iden-tical in Phyllostomus and Micronycteris. Thehorny papillae in these two genera form adistinctive 3/4 row (three anterior and fourposterior, see fig. 24A) and the circumvallatepapillae are all large and well developed. InMacrotus, the horny papillae show a less or-derly appearance (fig. 24B), and the two lat-eral circumvallate papillae are very reduced.

All five stenodermatine genera have a gen-erally similar tongue morphology. All havehorny papillae, singly-pointed (mostly fleshy)papillae, fungiform papillae, and four cir-cumvallate papillae. They also all share adistinctive cluster of bifid papillae located in

30 NO. 2742

u

I


FIG. 23. Dorsal surfaces of the tongues of Brachyphylla cavernarum (left) and Phyllonycteris poeyi(right). Bar = 1 mm. MCP = median circumvallate papilla, FP = fungiform papilla, HP = horny papilla,HLP = hairlike papillae.

the posteromedian region of the dorsaltongue surface (though this cluster is reducedin Vampyressa). The horny papillae of Uro-derma resemble those of Phyllostomus/Mi-cronycteris in having the 3/4 pattern (fig. 24);all other stenodermatines have a "less or-derly" Macrotus-type appearance (see fig.25). Interestingly, the three tongue types ob-served in the Stenodermatinae correspondwell to the three divisions of the Stenoder-matinae proposed by Gardner (1977).The tongue of Carollia is most similar to

the Glossophaga-type tongue in some char-acters. There are no hairlike papillae, but thehorny papillae consist of two large, poste-

riorly directed papillae, surrounded by sev-eral smaller papillae (fig. 26). There are nobifid papillae, but the remaining papilla typesof Glossophaga are present. There are fourcircumvallate papillae.The tongue of Desmodus is, in some re-

spects, most similar to the tongues of Lon-chophylla, Lionycteris, and Platalina. Thereare very few papilla types on the tongue sur-face: essentially there are only fleshy monofidpapillae and perhaps a few fungiform pa-pillae. No other type is present. Additionally,there is a longitudinal groove along the lateraltongue surface, though this groove is notnearly as deep as the one in the Lonchophylla

1982 3 1


0 0000

A B

FIG. 24. The horny papillae of Phyllostomushastatus (left) and Macrotus waterhousii (right).The major papillae are filled in to distinguish themfrom the minor papillae (ones that do not openposteriorly, see text). Bar = 1 mm.

group of bats. There are no hairlike papillaelining the groove in Desmodus, as there arein the Lonchophylla group.

INTERNAL HISTOLOGY

GLOSSOPHAGINAE: All glossophagines ex-amined except Lonchophylla, Lionycteris,and Platalina have a similar internal tonguemorphology (see figs. 27 and 28). Anteriorlyin the tongue, there is a single, midline lingualartery, rather than left and right lingual ar-

MCP

B~~~~BP

HP

FIG. 25. Dorsal surface of the tongue of thestenodermatine bat, Artibeusjamaicensis, with aninset of the horny papillae. Bars = 1 mm.MCP = median circumvallate papilla, BP = bifidpapillae, HP = horny papilla.

U1\____

FIG. 26. Dorsal surface of the tongue of Ca-rollia perspicillata and an inset of the horny pa-pillae. Bars = 1 mm. MCP = median circumval-late papilla, MP = monofid papillae, HP = hornypapilla.

teries as in most mammals. To either side ofthe artery are two large lingual veins, con-nected to the artery by artero-venous shunts.The horizontal lingual musculature passesaround each of these lingual veins (fig. 27),enclosing them. Toward the tip ofthe tongue,branches of the lingual veins pass laterallyand dorsally into the interior ofeach hairlikepapilla.The intrinsic tongue structure of the re-

maining three genera is shown in figure 29.Most prominent are the deep longitudinalgrooves on each side ofthe tongue. Undoubt-edly, the shape of these grooves is controlledby the complex bundles of skeletal musclethat pass in all directions within the tongue.There are left and right lingual arteries andveins, plus accessory arteries and veins in thedorsal part of the tongue.BRACHYPHYLLINAE: The intrinsic tongue

structure of Phyllonycteris and Erophylla isvery similar to that of the Glossophaga-likeglossophagines. There is a single, midline lin-gual artery connected by shunts to twoslightly enlarged lingual veins (fig. 31). Theintrinsic muscle bundles are also similar. InBrachyphylla, however, the tongue structureis more similar to the non-nectar-feedertongues described below (fig. 30). There aretwo lingual arteries and veins, with no sign

32 NO. 2742

GRIFHITHS: NECTAR-FEEDING BATS

LP

LA

FIG. 27. Cross section of the tongue of Glossophaga soricina.LA = lingual artery, LV = lingual vein, SM = skeletal muscle.

of the large shunts found in most glos- regions. Altsophagines. There is not a single, midline lin- characters Ngual artery present. (posterior slOTHER BATS: In all phyllostomines and developmer

stenodermatines studied, the intrinsic lingual loss of the cstructure is the same. There are two lingual gard these carteries and veins, with predominantly hor- ters ratherizontal skeletal muscle bundles passing same two claround them (fig. 32). In Carollia, these hor- dependentl)izontal muscle bundles are extraordinarily within the Iwell developed. In Desmodus, the tongue has gett, 1971,predominantly horizontal muscle bundles. that must EThere is a groove in the lateral tongue surface, The strongequite dissimilar to the groove of Loncho- Lionycteris,phylla, Lionycteris, and Platalina in that it dependentlyis not so deep, and there are no complex tongue morlmuscle bundles inserting on it. The tongue,

most ofthe ISYSTEMATIC CONCLUSIONS of other ph

horny andThe systematic relationships ofthe 16 gen- there are ha

era studied are presented in the cladogram, very differefigure 33. Tongue and hyoid apomorphies are sophaga-liksummarized in table 1. The traditional being concesubfamily "Glossophaginae" is clearly a di- face to formphyletic group, and the new subfamily are arranged"Brachyphyllinae" (proposed by Baker, 1979) and one linmay not be a valid group. The three genera dinal grooveLonchophylla, Lionycteris, and Platalina, ofthe tonguiheretofore regarded as glossophagines, have tongue strucmorphologically distinctive tongue and hyoid pare figs. 27

Bar = 1 mm. LP = lingual papilla,

though they share certain hyoidwith the "other glossophagines"hift of the sternohyoid origin andit of a sternoglossus complex byconnection to the basihyal), I re-characters as convergent charac-than as synapomorphies. Theharacter states have occurred in-y in at least three other groupsMammalia (see Doran and Bag-or Griffiths, 1978a) in animalshyperextend the tongue to feed.mst arguments for Lonchophylla,and Platalina having become in-y nectivorous can be seen in thephology (see figs. 21, 27, and 29).s of these three genera have lostpapilla types found on the tongueshyllostomids, most notably thecircumvallate types. Although

airlike papillae present, they arently arranged than in the Glos-;e glossophagines. Rather than,ntrated on the anterodorsal sur-a brush tip, the hairlike papillae

I in two lines, one line just dorsale just ventral to a deep longitu-e (see fig. 21) that runs the lengthe in all three genera. The internalcture is also very different (com-7 and 29). In Lonchophylla, Lio-

1 982 33


LAFIG. 28. Cross section ofthe tongue ofHylonycteris underwoodi. Bar = 0.5 mm. LP = lingual papilla,

LA = lingual artery, LV = lingual vein, SM = skeletal muscle.

nycteris, and Platalina, there are complexbundles of muscle running in many direc-tions within the tongue, probably to controlthe shape ofthe groove during nectar-feeding.These complex bundles are not present inother phyllostomids.

It is most unlikely that a bat line that haddeveloped this morphologically complextongue would lose these adaptations, andthen develop the equally complex tonguefound in Phyllonycteris, Erophylla, and theremaining glossophagines. It is thereforelikely that the common ancestor shared byLonchophylla/Lionycteris/Platalina and theother glossophagines was not a nectar-feeder,and that the two lines developed nectar-feed-ing independently. I thus propose that thegenera Lonchophylla, Lionycteris, and Pla-talina are an independently derived line,united by the synapomorphies of the tongue

(already described), and by: (1) M. crico-pharyngeus reduced to two, rather than threeslips; and (2) the posterior shift of the originof the sternohyoid and formation of a "ster-noglossus" complex. Note that certain othermuscle modifications such as posterior shiftof the insertion of the styloglossus, are pres-ent in the other nectar-feeding line, but notin this one. None of the characters I haveexamined distinguish Lonchophylla fromLionycteris, but Platalina has a slightlyshifted insertion ofthe genioglossus, and thusI show it as distinct on the cladogram. Twofinal points should be made about this line.First, because I have demonstrated that thereare non-glossophagines that are more closelyrelated to the Glossophaga-Choeronycterisgroup than are Lonchophylla, Lionycteris,and Platalina the last three genera must beplaced in a separate taxon of equal status to

34 NO. 2742


FIG. 29. Cross section of the tongue of Lonchophylla robusta. Bar = 1 mm. DA = dorsal artery,LA = lingual artery, LP = lingual papillae, LV = lingual vein, LG = longitudinal groove, SM = skeletalmuscle.

the Glossophaga-Choeronycteris group. Ithus must raise a new subfamily (see formal

classification below). Second, there may beother phyllostomids besides Brachyphylla,

1982 35


FIG. 30. Cross section of the tongue of Brachyphylla cavernarum. Bar = 1 mm. LA = lingual artery,LP = lingual papilla, LV = lingual vein, SM = skeletal muscle.

Phyllonycteris, and Erophylla that are alsomore closely related either to my newsubfamily, or the subfamily Glossophaginae(sensu stricto). I have left the base of thecladogram open to signify this very likelypossibility.The remaining 13 genera form what ap-

pears to be a monophyletic group. The genusBrachyphylla is the only possible exceptionto this statement. Other than the small pos-terior shift of the origin of the sternohyoid,there is no synapomorphy clearly unitingBrachyphylla with the Phyllonycteris-Choe-

ronycteris group. Brachyphylla does not pos-sess any of the complex internal or externaltongue modifications observed in the other12 genera. However, of all the bats examinedin this study, Brachyphylla is the most similarto what the primitive, non-nectivorousancestor of the other 12 might have lookedlike (for example, it has the proper hyoidbone morphology). For this reason, and be-cause Nagorsen and Peterson (1975), SilvaTaboada and Pine (1969), and Baker andBass (1979) have all suggested that there maybe a close relationship between Brachyphylla

36 NO. 2742


LP

LV

FIG. 31. Cross section of the tongue of Erophylla sezekorni. Bar = 1 mm.LP = lingual papilla, LV = lingual vein, SM = skeletal muscle.

and Phyllonycteris/Erophylla, I tentativelyplace Brachyphylla at the base of the clado-gram. The only other possible placementwould be on the same line with Phyllonyc-teris/Erophylla (it could be a non-nectivorederived from a nectivorous ancestor), but Ihave no evidence to support this view. I mustconclude that Brachyphylla is on a mono-generic line that is a sister-group to the Phyl-lonycteris-Choeronycteris group. Brachy-phylla cannot be placed in the same subfamilyas Phyllonycteris/Erophylla, as proposed byBaker (1979). For my arrangement, see myformal classification below, and see figure 33.

After Branching Point 1 on the cladogram,the remaining 12 genera are united by astrong set of synapomorphies. These are: (1)development of a single, midline lingual ar-tery, large lingual veins, and shunts connect-ing the two; (2) development of hairlike pa-pillae in a particular pattern on theanterodorsal tongue surface (a "brush-tip,"see figs. 21 and 23); and (3) a peculiar 2/1pattern of the major horny papillae (two pa-pillae anterior and one posterior) shared byPhyllonycteris, Erophylla, and the moreprimitive Glossophaginae (sensu stricto).

After Branching Point 2, there is a verystrong set of synapomorphies uniting Glos-sophaga-Choeronycteris. There is the poste-rior origin of the sternohyoideus from the

LA = lingual artery,

xiphisternum, and there is the elongation ofthe hyoglossus with the freeing of the ster-nohyoid-hyoglossus from the basihyal, form-ing a new "sternoglossus" complex. Both ofthese adaptations have been paralleled in theLonchophylla line of nectar-feeders. How-ever, the following derived character stateshave no parallels: (1) the styloglossus has aninsertion far posterior, on the posterior cor-ner of the tongue; and (2) the genioglossusinserts only into the posterior few mm. ofthetongue venter, rather than over the entireventral surface.

After Branching Point 3, there is a singlecharacter uniting the group Leptonycteris-Choeronycteris. Despite it being only a singlecharacter, it is a good synapomorphy thatclearly unites Leptonycteris-Choeronycterisas a holophyletic group. This character is thetunnel insertion of M. geniohyoideus, wherethe geniohyoideii completely envelop thehyoglossi (fig. 9). This derived conditioncould easily have developed from the genio-hyoid found in Glossophaga/Monophyllus!Lichonycteris (or for that matter, from thegeniohyoideus arrangement found in Lon-chophylla/Lionycteris/Platalina, though thetongue morphology is very different). I sug-gest that the expanded tunnel insertion ofthegeniohyoid in the Leptonycteris-Choeronyc-teris group would facilitate elongation of the

1982 37


LP

FIG. 32. Cross section of the tongue of Micronycteris nicefori. Bar = 0.5LP = lingual papilla, LV = lingual vein, SM = skeletal muscle.

contracted sternohyoid, thus aiding in ex-tending the tongue maximally (see fig. 10).Regardless of the functional reason for de-veloping the tunnel insertion, the conditionis apparently unique to this group; it has noteven been reported in the various othermammal groups that hyperextend the tongue(Doran and Baggett, 1971).The other line to the left at Branching Point

3 must also be justified since there is morethan one genus on the line. All three genera,Glossophaga, Monophyllus, and Lichonyc-teris possess the apomorphies at BranchingPoint 2, but do not have the tunnel insertionsynapomorphy of Branching Point 3. It isclear that all three genera are placed at theproper grade of glossophagine evolution, butunfortunately, the character states of thehyoid and tongue regions do not help hereto sort out the genera cladisticly. Glossophagaand Monophyllus are very similar in every

mm. LA = lingual artery,

respect and possibly should be combined inthe genus Glossophaga (Varona, 1974, doesthis). It is not surprising that the charactersof the hyoid and tongue regions fail to sep-arate them. The placement of Lichonycterisis more of a problem. Lichonycteris has beenplaced with Platalina/Hylonycteris/Sclero-nycteris (Gardner, 1977; and see Smith,1976); and with Hylonycteris alone (Phillips,1971). Additionally, there are certain dentalsimilarities to Leptonycteris, and Thomas(1895) suggested in the original generic de-scription that Lichonycteris resembled bothGlossophaga and Choeronycteris, especiallythe latter. The characters I have used in thisstudy suggest that Lichonycteris should notbe placed after Leptonycteris or before Phyl-lonycteris/Erophylla. I have placed it as anearly offshoot of the Glossophaga/Mono-phyllus line, rather than choosing the otheroption of placing it on its own monogeneric

38 NO. 2742


TABLE 1Summary of the Apomorphies Used in Constructing the Nectar-Feeding Bat Cladogram (fig. 33)

+ = presence of the character; 0 = absence of the character; +/0 = variable.

Derived Character State Br Ph Er GI Mo Li Le An Hy Ch Cht Lo Lio P1

1) post. shift ofsternohyoid origin + + + + + + + + + + + + + +

2) xiphoid origin ofsternohyoid 0 0 0 + + + + + + + + + + +

3) loss of sternohyoid'sconnection to hyoidbone 0 0 0 + + + + + + + + +/0 +/0 +

4) hyoglossus elongatedand loses connectionto hyoidbone 0 0 0 + + + + + + + + + + +

5) double insertion ofgeniohyoid 0 0 0 + + + + + + + + + + +

6) tunnel insertion ofgeniohyoid 0 0 0 0 0 0 + + + + + 0 0 0

7) post. shift ofstyloglossus insertion 0 0 0 + + + + + + + + 0 0 0

8) post. shift of seegenioglossus insertion 0 0 0 + + + + + + + + + + text

9) loss ofthe stylohyoid + 0 0 0 0 0 +/0 + + + + + + +10) reduction of sphc. col.

prof. 0 0 0 0 0 0 0 0 + + + 0 0 011) cricopharyn. reduced

to two bellies 0 0 0 0 0 0 0 0 0 0 0 + + +12) groove in tongue lined

w/ hairlike papillae 0 0 0 0 0 0 0 0 0 0 0 + + +13) almost complete loss

of ling. papillae 0 0 0 0 0 0 0 0 0 0 0 + + +14) brush tip formed by

hairlike papillae 0 + + + + + + + + + + 0 0 015) two medial CV

papillae absent 0 0 0 0 0 0 +/0 + + + + see text

16) horny papillae in 3/4pattern 0 0 0 0 0 0 0 0 + + + 0 0 0

17) single midline ling.art. 0 + + + + + + + + + + 0 0 0

18) enlarged ling. veins 0 + + + + + + + + + + 0 0 0

line either after or before the GlossophagalMonophyllus line. This decision is based noton lingual morphology, but rather for karyo-typic and dental reasons discussed in the nextsection.

After Branching Point 6, there are onlyminor characters uniting the Anoura-Choe-ronycteris group (and there are some dentalcharacters discussed in the next section that

suggest that the placement of Anoura in thisposition should be regarded as tentative). Thesynapomorphies after Branching Point 6 are:(1) complete loss of the two medial circum-vallate papillae; and (2) complete loss of M.stylohyoideus. Ashlock (1974) quite correctlypointed out that generally one should be sus-picious of "loss" characters on a cladogram.There is little question that Anoura belongs

1982 39


Cl)

cl 0) 0)Cl

01 C (.* CU mC

C.)% 0 Cl) a._C 0

_ ,. Q -;uCL C

C) *_ O- > Q

co m X 0 2C L- 0

-Ji a: CI 0. w aY 2

l)

.()

>

FIG. 33. Cladogram showing the relationships of the nectar-feeding genera discussed herein. See textfor characters used.

with Leptonycteris, Hylonycteris, Choero-niscus, and Choeronycteris but its placementon the cladogram merely shows the point itseems to fit best and, as with Lichonycteris,should be regarded as tentative.

After Branching Point 7, there are onceagain several strong synapomorphies that in-dicate that the Hylonycteris-Choeronycterisgroup is monophyletic. Scleronycteris andMusonycteris exist only as study skins in col-lections, so obviously I have not dissectedthem. I place them near what I believe aretheir closest relatives, based on my exami-nation of their teeth and basicranial regions.Synapomorphies of the entire group include:(1) a strong reduction of the sphincter colliprofundus muscle, and (2) the developmentofa complex 4/3 pattern ofthe horny papillae(see fig. 22) that is unique to this group ofglossophagines. Additionally, Phillips (1971)reported, and I confirm here, that the generaof the Hylonycteris-Choeronycteris groupshare an unusual and highly derived basi-cranial morphology, where the pterygoid pro-cesses are strongly inflected and contact the

auditory bullae posteriorly. There are otherdental and karyotypic data uniting this group,discussed below.The remaining three genera are all closely

related, probably having become genericallydistinct comparatively recently. The char-acters of the hyoid and lingual regions areinsufficient to distinguish between them, andso I must rely on dental and karyotypic ob-servations, discussed below.

SUPPORTING EVIDENCE FROMOTHER DISCIPLINES

The analyses of the karyotypic and dentaldata have produced apparently conflictingphylogenies for the subfamily Glossophag-inae (see figs. 1 and 2). The purpose of thissection is to reexamine these data, and showthat they support the cladogram presentedhere as well as they support the phylogeniesconstructed by Phillips (1971) and Gardner(1977).Upper Incisors: Evidence from the exam-

ination of the glossophagine upper incisors

=

m0

-c

0

Cl) __

C- >%

0Cl00-3

40 NO. 2742


(Winkelmann, 1971; Phillips, 1971) and myown personal observations support the clado-gram I present here. The incisors of Loncho-phylla, Lionycteris, Platalina, and Glos-sophaga are the least reduced, or mostprimitive. They resemble the upper incisorsof Brachyphylla, Phyllonycteris, and Ero-phylla in that the inner incisors are notablylarger than the outer ones, and have broadcutting edges (Phillips, 1971), whereas theouter incisors are more pointed. Monophyllusand Leptonycteris also have "relatively un-reduced" upper incisors (Phillips, 1971),though the inner pair is reduced to the samesize as the outer pair. Apparently because ofthis reduction, a small gap has developedbetween the two inner incisors of these twogenera (see Winkelmann, 1971). The trendfor reduction ofthe incisors continues throughAnoura and Hylonycteris to Choeroniscus,Choeronycteris, and Musonycteris where theinner incisors are small, peglike teeth sepa-rated by a wide gap, and the outer incisorsare reduced as well. Interestingly, the upperincisor configuration of Lichonycteris is anadditional strong argument against placingthis genus with Hylonycteris, Choeroniscus,or Choeronycteris. The upper incisors of Li-chonycteris are reduced, but in a differentmanner. The inner incisors are broad and theouter incisors are pointed, as in Glossophaga.There is almost no gap between the innerincisors (though they are very reduced), asthere is in all the more advanced glos-sophagines. The incisors of Lichonycteriscould be most easily derived from those ofPhyllonycteris, Erophylla, or Glossophagathough, of course, the condition in these batsis primitive for the subfamily as a whole. Thedifferently reduced incisors in Lichonycteriscan only be used to emphasize the lack ofrelationship to the Hylonycteris-Choeronyc-teris group. Unfortunately, there is no goodincisor synapomorphy uniting the Glos-sophaga/Monophyllus line and Lichonyc-teris.Upper Canines: In Lonchophylla, Lionyc-

teris, Brachyphylla, Phyllonycteris, Ero-phylla, Glossophaga, Monophyllus, Lepto-nycteris, and Anoura, the canines areunreduced, with a prominent cingular style(Phillips, 1971, and personal observ.). Thecanines are reduced in Platalina, Lichonyc-

teris, and the Hylonycteris-Choeronyc-teris group. If my cladogram is correct, theupper canines would have had to become re-duced independently three times: once inPlatalina, once in Lichonycteris, and once inthe Hylonycteris-Choeronycteris group. Thereis no evidence for or against this view.Upper Premolars: The upper premolars are

all simple, primitive teeth in Lonchophylla,Lionycteris, Glossophaga, Monophyllus, andLeptonycteris (Phillips, 1971). Anoura hassimilar upper premolars, but possesses a per-manent P2, which is probably a duplicatedP3 (Koopman, personal commun.), and thusnot of great taxonomic significance. The re-maining genera (Platalina, Lichonycteris,Hylonycteris, Scleronycteris, and the Choe-ronycteris/Choeroniscus group) all have spe-cialized upper premolars (Phillips, 1971).The Choeronycteris/Choeroniscus line hasbecome extremely specialized, with the pre-molars reduced to long, thin teeth. Hylo-nycteris and Lichonycteris show similar re-ductions, with the loss ofvarious shelves andstylar elements, which caused Phillips (197 1)to group the two genera together (see fig. 2).This would not be permitted in a cladisticanalysis, however, because as Phillips (1971)himself pointed out, the second upper pre-molar in Lichonycteris retains the primitive"postero-lingual shelf' and the "small ante-rior and posterior styles" as in the less de-rived, Glossophaga-like teeth. I believe thatthe more primitive tooth morphology of Li-chonycteris argues against including Licho-nycteris with the more advanced glossopha-gines.Upper Molars: Phillips (1971) used differ-

ences he observed in the configuration of theupper molars as a primary means of classi-fication of the glossophagines. I suggest thatthe upper molar configurations support mycladogram (fig. 33) at least as well as theysupport his phylogenetic tree (fig. 2). Plata-lina, Hylonycteris, Scleronycteris, Choero-niscus, and Choeronycteris all share the de-rived character of obliteration of the anteriorhalf of the W-shaped ectoloph (found in themore "primitive" glossophagine genera). Re-moval of Platalina from the group (which Ihave shown elsewhere to be not closely re-lated to the others) allows the use ofthis char-acter as a synapomorphy uniting the genera

1982 41


after Branching Point 7 on my cladogram.The primitive W-shaped ectoloph is promi-nent in Glossophaga, Monophyllus, and An-oura but in Leptonycteris the anterior half isconsiderably straighter than in the Glos-sophaga ectoloph. This straightening couldbe considered a precursor to the condition inthe Hylonycteris-Choeronycteris group,though Anoura, which retains the prominentW-shaped ectoloph, would have to be movedout ofthe Leptonycteris-Choeronycteris groupif this character were found to be significant.Once again, Lichonycteris retains the primi-tive state of a character, which suggests thatit does not belong among the more advancedgenera.Lower Incisors: The lower incisors are

completely absent in Lichonycteris, Anoura,Hylonycteris, Scleronycteris, Choeroniscus,Choeronycteris, and Musonycteris (Phillips,1971, and personal observ.). In Loncho-phylla, Lionycteris, and Platalina, the lowerincisors are very large, flat teeth (Phillips,1971; Winkelmann, 1971) with distinctive"trifid" crowns (Phillips, 1971). These dis-tinctive incisors can be used as a synapo-morphy uniting the above three genera. Thelower incisors are present (primitive condi-tion) in Glossophaga, Monophyllus, and Lep-tonycteris. Except for the condition in Li-chonycteris (which would have to be theresult of convergence), these data could beinterpreted as a synapomorphous character(loss oflower incisors) uniting the genera afterBranching Point 6 on my cladogram.Lower Canines: The lower canines ofevery

genus to the right of Branching Point 7, plusLichonycteris, are reduced. This reductioncould be considered a synapomorphy unitingthe Hyloncteris-Choeronycteris group. Again,Lichonycteris would have had to develop thecondition independently.Lower Premolars: There is considerable

variation in premolar morphology among thevarious genera (Phillips, 1971). In my opin-ion, the only good synapomorphy uniting agroup is the character of long, thin premolarsfound in Choeroniscus, Choeronycteris, andMusonycteris (see Phillips, 1971); this wouldunite the group above Branching Point 8.Lower Molars: The lower molars of all

glossophagine genera are remarkably similar(Phillips, 1971). In Musonycteris and Choe-

ronycteris the molars are long and thin, witha "flange" on the postcristid (Phillips, 1971)which is present, though underdeveloped inChoeroniscus. This character can be used tounite Choeronycteris and Musonycteris aboveBranching Point 9 on the cladogram.

Basicranial Region: Phillips (1971) cor-rectly reported that the pterygoid processesof Choeroniscus, Choeronycteris, and Mu-sonycteris have an inflected tip that comes incontact with the auditory bullae. Addition-ally, Hylonycteris has a slightly inflected re-gion that could be considered a precursor tothat above. Phillips (1971) used the pterygoidcharacter (and several upper molar charac-ters) to divide the glossophagines into a"Choeronycteris group" and a "Glossophagagroup." The condition noted in the Choe-ronycteris group is clearly a synapomorphythat unites Choeroniscus-Musonycteris, andHylonycteris-Musonycteris (if the conditionin Hylonycteris is a valid precursor). Phil-lips's "Glossophaga group" is not a validgroup because the pterygoids of all these batsare primitive (except for Anoura, which in afew cases shows some pterygoid inflection).Phillips (1971) was thus using a symplesio-morphic condition to unite a group.

Karyology: Unfortunately, because of therarity of many of the species of the Glosso-phaginae, some genera have not been karyo-typically examined. Additionally, only a fewhave been examined with the G and C band-ing techniques now available (see Baker andBass, 1979). The karyotypic data availablecan be interpreted to support the cladogrampresented here.

Baker (1967, 1973, 1979) proposed thatthe primitive karyotype for phyllostomidbats is: diploid number (2n) = 30-32, fun-damental number (FN) = 56-60. If this bethe case, then Brachyphylla, Phyllonycteris,Erophylla, Glossophaga, Monophyllus, andLeptonycteris would share the least derived(32/60) karyotype within the nectar-feedercomplex. The Lichonycteris karyotype (either28/50 or 24/44, Baker, 1979) is most similarto, and most easily derivable from, the karyo-type ofone ofthe above bats (I have suggestedfrom the Monophyllus/Glossophaga line), asGardner (1977) illustrated. The remaininggenera (Anoura-Choeronycteris), with succes-sively decreasing 2n and FN's (see Baker,

42 NO. 2742


1979) can be derived from this Glossophaga-like karyotype (Baker, personal commun.).The arrangement I present (fig. 33) also ex-plains why the karyotypes of Lonchophyllaand Lionycteris are so different from thoseof the "other glossophagines" (Platalina hasnot yet been karyotyped), as Gardner (1977)showed. Baker (personal commun.) hasstated that it would take a large number ofchromosomal rearrangements to derive thekaryotypes of Lonchophylla and Lionycterisfrom the "other glossophagines"; this is eas-ily explained by my suggestion that the "lon-chophylline" bats are not closely related tothe glossophagines (sensu stricto).Summary and Formal Classification: Ex-

cept for some problems in the dentition ofLichonycteris, the karyotypic, dental, andhyoid/lingual data can be interpreted to sup-port the cladogram presented here (fig. 33).I stress that although there may be problemswith the exact placement ofLichonycteris andpossibly Anoura, the available evidencestrongly supports the monophyly ofthe Glos-sophaginae (minus Lonchophylla, Lionyc-teris, and Platalina), the distinctiveness andmonophyly of the three lonchophylline gen-era, the monophyly of the Phyllonycteris-Choeronycteris group, the monophyly of theLeptonycteris-Choeronycteris group, and themonophyly of the Hylonycteris-Choeronyc-teris group. The overall form of the clado-gram is probably correct, though Lichonyc-teris and Anoura may be slightly misplaced.

I am opposed to the hierarchical classifi-cation presented by many cladists, whereeach branch of the cladogram must be des-ignated as a higher taxonomic group. Usingthis method, making the slightest change onany level disturbs the stability of the classi-fication. I am also in favor of the principleof disturbing the current classification theleast when making changes. The simplestmethod of following both precepts is pre-sented below.

Family PhyllostomidaeSubfamily PhyllostominaeSubfamily StenodermatinaeSubfamily CarolliinaeSubfamily DesmodontinaeSubfamily BrachyphyllinaeBrachphylla

Subfamily PhyllonycterinaePhyllonycterisErophylla

Subfamily GlossophaginaeGlossophagaMonophyllusLichonycterisLeptonycterisAnouraHylonycterisScleronycterisChoeroniscusChoeronycterisMusonycteris

NEW SUBFAMILYSubfamily LonchophyllinaeLonchophyllaLionycterisPlatalina

Because of the distinct differences in toothmorphology between the phyllonycterinesand glossophagines, I am not now in favorof including Brachyphylla, Phyllonycteris,and Erophylla in the subfamily Glossophag-inae, though this may eventually be done(perhaps at the Tribe level). For now, I haveapplied the traditional classification systemto my results recognizing that Brachyphyllacannot be considered a member of the Phyl-lonycterinae under the rules of cladistic clas-sification. The only option available untilsuch time as it might be included in the Glos-sophaginae is to relegate it to its own mono-generic subfamily Brachyphyllinae (nameproposed by Baker, 1979).

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