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AMERICAN MUSEUM Novitates PUBLISHED by the AMERICAN MUSEUM of NATURAL HISTORY CENTRAL PARK WEST at 79TH STREET, NEW YORK, N.Y AMERICAN MUSEUM Novitates PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL 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 the vory observed. The other group, comprising the hyoid and lingual regions of the New World nec- remaining 10 glossophagine genera (Glossopha- tar-feeding bats reveal marked modification ofthe ginae, sensu stricto), plus Phyllonycteris, Ero- tongue retractor musculature (Mm. sternohyoi- phylla, and perhaps Brachyphylla form a mono- deus, geniohyoideus, hyoglossus, styloglossus, and phyletic group. Within the newly restricted genioglossus) and modification ofthe internal and subfamily Glossophaginae there are two major external tongue structure from the conditions clades. One clade is composed of Glossophaga, found in non-nectar-feeding bats. Use of these Monophyllus, and surprisingly, Lichonycteris. The derived characters in a cladistic analysis leads to other is composed of the more derived nectar- the phylogenetic hypothesis that nectivory evolved feeding genera: Leptonycteris, Anoura, Hylonyc- twice independently in the family Phyllostomidae. teris, Choeroniscus, Choeronycteris, and probably One group of nectar-feeding phyllostomids, com- Scleronycteris and Musonycteris. Interestingly, prising the genera Lonchophylla, Lionycteris, and both karyotypic evidence, and evidence from den- Platalina (traditionally considered glossopha- tal and basicranial studies, can be interpreted to gines) deserves separate subfamilial status based support the phylogeny presented here. on the markedly different adaptations for necti- INTRODUCTION For almost 15 years the systematic status 1973; Baker and Lopez, 1970; Gerber and of the New World nectar-feeding bats Leone, 1971; Phillips, 1971; Stock, 1975; (subfamily Glossophaginae) has been dis- Gardner, 1977; Baker and Bass, 1979; Baker puted. Baker (1967) first suggested that the et al., 1981) have continued to examine this subfamily Glossophaginae might not be a question, but while many investigators agree monophyletic group on the basis ofhis karyo- that the group is probably not monophyletic, typic studies of several genera of the group. there is little agreement as to exactly how the Since then Baker and others (see Baker, 1970, group 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 2 AMERICAN MUSEUM NOVITATES NO. 2742 In addition to the comparatively large Within the Phyllostominae, he recognized subfamily Glossophaginae, there is a smaller four "groups": the Vampyri, the Glossopha- group of endemic Antillean genera that are gae, the Stenodermata, and the Desmo- at least partly nectivorous. These genera have dontes. The Glossophagae contained 10 been traditionally placed in a separate species in seven genera. These genera were subfamily, the Brachyphyllinae (=Phyllo- Glossophaga, Phyllonycteris, Monophyllus, nycterinae, Miller, 1907). However, recent Ischnoglossus (=Leptonycteris), Loncho- karyological work (Baker and Bass, 1979) and glossa (=Anoura), Glossonycteris (=Anoura), immunological work (Baker et al., 1981) in- and Choeronycteris. dicated that the Brachyphyllinae may be The "group" Glossophagae was considered closely related to Glossophaga and Mono- distinct from all other phyllostomids on the phyllus (both glossophagines). This finding basis of: (1) the long, narrow muzzle; (2) the led Baker and Bass (1979) to question the long, extensible tongue "clothed with filiform validity of the subfamily Brachyphyllinae, papillae"; and (3) the deep groove in the and to once again suggest that the Glosso- lower lip. Except for the inclusion of Phyl- phaginae might not be a monophyletic group. lonycteris, today considered to be grouped The hyoid and lingual regions of the glos- with Brachyphylla and Erophylla in a sepa- sophagine bats are highly modified (Sprague, rate, endemic Antillean subfamily, the 1943; Wille, 1954; Winkelmann, 1971; "group" Glossophagae includes all the bats Greenbaum and Phillips, 1974; Howell and then known that are today considered to be- Hodgkin, 1976; Griffiths, 1978a) presumably long to the subfamily Glossophaginae. to permit the hyperextension of the tongue Miller (1907) reexamined the species required for nectar-feeding. These modifi- known to Dobson, plus specimens in the cations are complex and extensive, and thus United States National Museum and mu- are ideal for use as derived characters (apo- seums in Paris, Leiden, and Berlin. Basing morphies, Hennig, 1966) in a cladistic study. his classification on the structure ofthe wing, The main purpose ofthis paper is to attempt sternum, shoulder girdle, and tooth cusps, to resolve the question of the monophyly of Miller divided the Chiroptera into two sub- the subfamily Glossophaginae via dissection orders, 17 families, and 19 subfamilies. All of the hyoid region and histological exami- subsequent classifications of the Chiroptera nation of the tongue. Secondary purposes are based on Miller's work, including Simp- include resolving the exact systematic rela- son (1945), Hall and Kelson (1959), Koop- tionship of the three genera of the other man and Cockrum (1967), Koopman and nectar-feeding subfamily (Brachyphyllinae) Jones (1970), Smith (1976), and Hall (1981). to the Glossophaginae, and determining the Miller (1907) divided the family Phyllostom- relationships of the genera within each idae into seven subfamilies: the Chilonycter- subfamily to one another. To accomplish inae (=family Mormoopidae, Smith, 1972), these goals, representative species of each Phyllostominae, Stenoderminae, Phyllonyc- genus of glossophagine (except Musonycteris terinae (=Brachyphyllinae, Baker, 1979), and Scleronycteris, which were unavailable) Hemiderminae, Sturnirinae, and Glosso- were dissected and compared with represen- phaginae. Miller (1907) recognized that Phyl- tative species ofeach genus ofbrachyphylline lonycteris, "Reithronycteris" (=Phyllonyc- bat, and with a variety of species ofnon-nec- teris, Koopman, 1952), and Erophylla tar-feeding phyllostomid bats. deserved separate subfamilial status on the basis of the "peculiar" tooth structure and HISTORY OF THE PROBLEM the modified noseleaf. Miller also added the The first attempt at a unified classification genera Lonchophylla, Hylonycteris, and Li- of a large number of New World bats was chonycteris to the subfamily Glossophaginae, that of Dobson (1878). Dobson recognized and recognized Dobson's "Ischnoglossa" and two subfamilies within the family Phyllo- "Glossonycteris" as Leptonycteris and An- stomidae: the Lobostominae (=Mormoopi- oura, respectively. With the addition of five dae, Smith, 1972) and the Phyllostominae. more genera (Scleronycteris, Thomas, 1912; 1 982 GRIFFITHS: NECTAR-FEEDING BATS 3 Lionycteris, Thomas, 1913; Choeroniscus, immunologic reactions of sera of glossoph- Thomas, 1928; Platalina, Thomas, 1928; agine bats, also suggested that the Glosso- and Musonycteris, Schaldach and Mc- phaginae were an artificial grouping ofnectar- Laughlin, 1960), the subfamily Glossophag- feeders. They too suggested that there was a inae was generically complete as it is tradi- distinct Glossophaga group and a distinct tionally recognized today. Choeronycteris group. However, relation- However, recent investigations in the areas ships of these groups to non-glossophagines ofchromosome morphology, immunological were directly opposite to those suggested by reactions ofblood sera, and hard morphology Baker (1967). Glossophaga soricina and of the basicranial skull and teeth have given Glossophaga commissarisi were immunolog- rise to speculation that the classic "Glosso- ically more closely related to Carollia than phaginae" may not be a monophyletic group. to Choeronycteris; Choeronycteris mexicana Baker (1967, 1970), on the basis of chro- was most closely related to Phyllostomus, mosome morphology, suggested that Lepto- Chrotopterus (both phyllostomines), and sur- nycteris sanborni, Glossophaga soricina, G. prisingly, to Desmodus, the vampire bat. alticola, and G. commissarisi form a distinct Recent electrophoretic and albumin immu- group which may be more closely related to nological work by Baker et al. (1981) seem Phyllostomus hastatus, Macrotus water- to contradict the karyotypic studies further. housii, and Trachops cirrhosus (all subfamily Baker et al. (1981) presented evidence that Phyllostominae) than to two other glossoph- Anoura, Glossophaga, Monophyllus, Lepto- agines: Choeronycteris mexicana and Choe- nycteris, Hylonycteris, and Choeroniscus form roniscus godmani. Baker (1967) hypothe- a clade. This suggestion directly contradicts sized that the Glossophaginae may actually the karyotypic studies (see Baker, 1967; be an artificial grouping of nectar-feeders, Baker and Bass, 1979) that suggest the Glos- evolved from two or more independent lines. sophaginae are not monophyletic. Choeronycteris and Choeroniscus karyotypi- Stock (1975) contributed to the Baker/Ger- cally showed great similarity to Carollia sub- ber and Leone controversy by reexamining rufa and Carollia perspicillata (subfamily chromosomes of Carollia and Choeroniscus Carolliinae), whereas another glossophagine, using G and C banding techniques. Stock Anoura
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