The chiropteran premaxilla : a reanalysis of morphological variation and its phylogenetic interpretation

2007·2.5 MB·English

by  Giannini, Norberto P

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Novitates
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CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3585, 44 pp., 35 figures, 1 table September 6, 2007
The Chiropteran Premaxilla: A Reanalysis of
Morphological Variation and Its
Phylogenetic Interpretation
NORBERTO P. GIANNINI1,2 AND NANCY B. SIMMONS1
ABSTRACT
The mammalian premaxilla, which bears the incisor teeth, is composed of a body and two
processes (nasal and palatine) that articulate with other rostral bones via four cranial sutures. In
bats, the premaxilla is modified in many ways, and this variation has been extensively used in bat
systematics. The premaxilla has provided characters to diagnose a number of important taxonomic
groupings—most notably, the division of Microchiroptera into the infraorders Yinochiroptera and
Yangochiroptera. Recent molecular studies have challenged the monophyly of Microchiroptera,
and several families have been transferred to clades other than those in which they were placed
traditionally. Because premaxillary characters have figured prominently among those used to
establish the traditional classification of bats, we compared the anatomy of the bone across
suprageneric bat groups and provide revised descriptions of its variation. On the basis of extensive
material examined, we generated 16 new characters, of which at least 12 are partially applicable to
all Chiroptera, and several of which are informative within specific bat groups. Three new
characters code variation in the basic structure of the chiropteran premaxilla in a new way. As
a result, the traditional character defining Yinochiroptera (a “movable premaxilla”) was found to
lack an anatomical basis; by contrast, Yangochiroptera was still supported. Still, a tree search
using just the new premaxillary characters recovered Yinochiroptera as monophyletic. Even with
a low character-to-taxon ratio, premaxillary characters recover a number of clades recognized in
recent phylogenetic studies of bats. Mapping of characters onto the latest molecular and
morphological chiropteran trees required many more extra steps in the former than in the latter.
Our interpretation of premaxillary variation in bats suggests two opposing trends in different
lineages: one toward weakening and eventual loss of the bone, and the other toward a strengthening
1 Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History (npg: [email protected]; nbs:
[email protected]).
2 PIDBA, CONICET, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucuman,
Argentina.
Copyright © American Museum of Natural History 2007 ISSN 0003-0082
2 AMERICAN MUSEUM NOVITATES NO. 3585
via suture fusion. We conclude that, despite some homoplasy, the chiropteran premaxilla is richer
in potentially phylogenetically informative characters than previously thought and that it should
be explored further in systematic studies of bats at a variety of systematic levels.
INTRODUCTION
The premaxilla is a paired dermal bone
located at the apex of the rostrum of the
vertebrate skull. It typically bears the anterior
teeth, which in mammals are the incisors, and
it plays an important functional role in food
acquisition and processing. The mammalian
premaxilla, or incisive bone (os incisivum;
fig. 1), is composed of the body (corpus ossis
incisivi; sometimes called alveolar process), the
nasal process (processus nasalis), and the
palatine process (processus palatinus; Evans,
1993). The body of the premaxilla bears the
alveoli for the incisors. The nasal process is
a roughly vertical, compressed projection from
the body that forms the lateral side of the
external nasal aperture. The palatal process
forms the anteriormost part of the hard palate.
Each palatine process typically bears an in¬
cisive foramen, which divides the palatine
process into a medial flange (running along
the midsagittal line) and a lateral flange
(running alongside the alveolar line). Most
frequently, the caudal edge of each incisive
foramen is delimited by the maxilla (fig. 1). The
premaxilla participates in four cranial sutures:
the interincisive suture (sutura interincisiva),
nasoincisive suture (sutura nasoincisiva), max-
illoincisive suture (sutura maxilloincisiva), and
vomeroincisive suture (sutura vomeroincisiva).
This basic plan of the mammalian pre¬
maxilla has been significantly modified in
many bat lineages, and Chiroptera contains
instances of variation not seen in most other
mammalian orders. Some aspects of this
osteological diversity have been described
previously (see Miller, 1907; Andersen, 1912;
Wible and Novacek, 1988; Simmons, 1994);
and the chiropteran premaxilla has yielded Fig. 1. Phyllostomus hastatus AMNH 17032,
characters of phylogenetic relevance that have ventral (A) and dorsal (B) view of the rostrum
been used in bat systematics at a variety of showing parts and sutures of the premaxilla. Scale
= 1 mm. Abbreviations: bp body of premaxilla; C
hierarchical levels. Premaxillary morph¬
upper canine; II first upper incisor; 12 second upper
ology has provided synapomorphies for
incisor; ifo incisive foramen; dI2 deciduous second
Chiroptera (e.g., Wible and Novacek, 1988;
incisor; iisu interincisive suture; mfpp medial flange
Simmons, 1994) and supported hypotheses of
of palatine process of premaxilla; mx maxilla; mxisu
key interfamilial relationships (e.g., Miller, maxilloincisive suture; na nasal; naisu nasoincisive
1907; Koopman, 1985, 1994; Simmons, 1998; suture; nap nasal process of the premaxilla; palp
Simmons and Geisler, 1998). The division of palatine process of the maxilla.
2007 GIANNINI AND SIMMONS: CHIROPTERAN PREMAXILLA 3
Microchiroptera into the infraorders Yino- Depending on the availability of specimens,
chiroptera and Yangochiroptera (Koopman, we complemented our analysis with observa¬
1985) was primarily based on differences in tions of isolated premaxillae from disarticu¬
premaxillary morphology. According to lated skulls and with images (sequences of
Koopman (1985, 1994), yinochiropteran bats slices and three-dimensional renderings) gen¬
bear a “movable premaxilla” that is only erated from computed tomography (CT)-
loosely attached to the maxilla; in contrast, scanned skulls at the University of Texas
yangochiropteran bats have a premaxillasol- High-Resolution X-ray CT Facility in Austin,
idly fused to the maxilla. Premaxillary char¬ Texas. (See details of the scanning technique
acters also provide diagnostic characters for in Rowe et al. [2005] and Macrini et al.
many chiropteran families and higher clades, [2006].) Low-resolution images of CT-scanned
including Craseonycteridae, Megadermatidae, skulls used in this study are available at www.
Nycteridae, Rhinolophidae + Hipposideridae, digimorph.org.
Emballonuridae, Rhinopomatidae, and Noctil- Our goal was to describe the structures and
ionidae (Miller, 1907; Hill, 1963, 1974; Koop¬ relationships determined by the three parts of
man, 1994; Simmons, 1998; Simmons and the premaxilla (body, nasal process, and
Conway, 2001). Within families, variation in palatine process) and the four sutures in which
the premaxilla has proved important in di¬ the premaxilla participates (incisive, nasoinci-
agnosing genera and species—for instance, in sive, maxilloincisive, and vomeroincisive su¬
Pteropodidae (e.g., Andersen 1912; Bergmans, tures), as well as traits that show interspecific
1997), Vespertilionidae (Koopman, 1994), and variation of importance, such as borders,
Molossidae (Koopman, 1994). Giannini and surfaces, and additional processes of the
Simmons (2005) used nine premaxillary char¬ premaxilla. In adult individuals of many bat
acters in a combined morphology and DNA species, the premaxilla is fused to neighboring
phylogenetic analysis of megachiropteran bat bones (maxilla, nasal, and vomer). Whenever
relationships. possible, we also examined young and sub¬
The aim of this contribution is to study the adult specimens in which the premaxillary
morphological diversity of the chiropteran sutures were still visible. Anatomical termi¬
premaxilla focusing on the potential phyloge¬ nology follows Giannini et al. (2006). We
netic utility of observed variation. We show examined specimens from the following col¬
that the variation of premaxillary structures in lections: American Museum of Natural
bats has not been fully documented and that History (AMNH); Carnegie Museum of
alternative interpretations of structures are Natural History, Pittsburgh (CM); Coleccion
necessary. Those interpretations, in turn, Mamiferos Lillo, Tucuman, Argentina
affect the ability to diagnose chiropteran (CML); Field Museum of Natural History,
clades as currently understood. Our compre¬ Chicago (FMNH); Louisiana State University
hensive descriptions of premaxillary osteology Museum of Zoology, Baton Rouge (LSU);
across bat groups facilitates redefinitions of Royal Ontario Museum, Toronto (ROM); and
previously described phylogenetic characters U.S. National Museum of Natural History,
as well as accurate definitions of new char¬ Smithsonian Institution, Washington, D.C.
acters. This analysis has immediate impact on (USNM). Some specimens are cited in specific
the phylogenetic reconstruction and classifica¬ context in the family accounts; however, much
tion of Chiroptera. larger series of specimens were actually
examined for the present study.
The observed variation in the form of the
premaxilla within Chiroptera far exceeds that
MATERIALS AND METHODS
known within any other mammalian order
We studied the osteology of the premaxilla and offers great potential for systematic
in selected species representing all currently analysis at all taxonomic levels. Toward this
recognized bat families, as well as principal end, we define here 16 phylogenetic characters
groups within families. We examined articu¬ that describe this variation and may be
lated premaxillary bones in adult specimens. employed in future phylogenetic analyses.
4 AMERICAN MUSEUM NOVITATES NO. 3585
Several premaxillary characters have been Default constant of concavity (k = 3) was
used in one form or another in previous used. All analyses were run in the program
phylogenetic analyses; we report prior descrip¬ TNT (Goloboff et al., 2004).
tions and discuss additional observations and
modifications, as appropriate. Other charac¬
RESULTS
teristics of the upper incisor dentition, such as
presence of each tooth, crown structure, and The Premaxilla across Bat Groups
deciduous replacement, are treated elsewhere
Pteropodidae: In all megachiropterans,
(Giannini and Simmons, 2007).
the palatine process of the premaxilla is
Three of the phylogenetic characters pro¬
missing altogether (Andersen, 1912). As a re¬
posed here (characters 1-3) describe major
sult, the incisive foramina coalesce in a single
alterations in premaxillary form that appear to
large opening, the incisive fissure (fig. 2; see
be informative at higher taxonomic levels.
also Giannini et al., 2006). Interspecific
These are each mapped onto the two most
variation in form of the premaxilla is thus
complete (in terms of taxonomic and character
limited to the body and nasal process, which
sampling) existing phylogenies, one based on
are present in all species. Interspecific varia¬
molecular data (Teeling et al., 2005) and the
tion is nevertheless substantial; Giannini and
other based on morphological data (Gunnell
Simmons (2005) identified nine characters of
and Simmons, 2005). Teeling et al. (2005) used
the premaxilla in megabats, which are briefly
13.7 kilobase pairs (kbp) from 17 nuclear
discussed here.
genes, and Gunnell and Simmons (2005)
Several methods have been used to describe
scored 204 characters from diverse organ
the relative width of the nasal process, which is
systems. Although other molecular and mor¬
phological phylogenies are available, they are
based on smaller data sets (e.g., Eick et al.
[2005] sampled 4 kpb from four nuclear
introns and did not include representatives of
all bat families) and thus were not employed in
the current study. Using the Teeling et al.
(2005) and Gunnel and Simmons (2005)
phylogenies as frameworks, we compare the
homoplasy (extra steps) required by each
phylogenetic hypothesis and reconstruct the
morphological evolution of the chiropteran
premaxilla. In addition, we have included all
16 characters in two phylogenetic analyses.
Taxonomic sampling was based on both
Teeling et al. (2005) and Gunnell and
Simmons (2005); additional taxa were includ¬
ed to represent observed variation in pre¬
maxillary characters. Two parsimony analyses
were performed, under equal and implied
weights, executing in each analysis 200 repli¬
cations of random addition sequences of taxa,
followed by Tree Bisection Reconnection
branch swapping. The implied weights analy¬ Fig. 2. Pteropus lylei CM 87972, ventral view of
anterior palate showing incisive fissure. Scale =
sis (Goloboff, 1993) resolves character conflict
2 mm. Abbreviations: II first upper incisor; 12
in favor of characters with less homoplasy,
second upper incisor; if incisive fissure; C upper
generally resulting in improved resolution and
canine; mxisu maxilloincisive suture; PI first upper
support (Goloboff et al., in press). The
premolar; P3 third upper premolar; palp palatine
analysis calculates individual character weight process of maxilla; v vomer (incisive incisure); vnc
by fitting a concave function of homoplasy. ventral nasal concha or maxilloturbinate.
2007 GIANNINI AND SIMMONS: CHIROPTERAN PREMAXILLA 5
a character long used in megachiropteran
systematics (see Andersen, 1912). We find
that variation in dorsal width is best reflected
in the extent to which the nasal process
articulates with the nasal, if it does so at all
(Giannini and Simmons, 2005: character 81).
The nasoincisive suture is long in Notopteris
and Melonycteris (fig. 3A). Andersen (1912)
used this character state in the diagnosis of his
Notopterine section, noting that this is the
presumed primitive condition in therians. The
remainder of megachiropteran genera show
three alternative states that reflect degrees of
reduction of the nasal process: an intermediate
condition in which the nasal process does not
distinctly vary in width from its ventral to its
dorsal extent and the nasoincisive suture is
of intermediate length (e.g., rousettines and
pteropodines; fig. 3B); a point contact, in
which the premaxilla tapers to a point that
just touches the anterior edge of nasals (e.g., in
most cynopterines and harpyionycterines,
some epomophorines; fig. 3C); and no con¬
tact, in which the premaxilla tapers to a point
that does not reach the nasal (in nyctimenines;
fig. 3D). The caudal edge of the nasal process
(the lateral or rostral component of the
maxilloincisive suture) may be gently curved,
as in most megachiropterans, or it may show
a right-angled maxilloincisive suture, as in,
for instance, P ter opus and Acerodon (fig. 4;
Giannini and Simmons, 2005: character 82).
The anterior edge of the nasal process, or the
lateral margin of the external nasal
aperture, projects forward in Nyctimene,
Paranyctimene, Megaerops, and Otopteropus,
whereas it does not do so in other genera
(Giannini and Simmons, 2005: character 86;
see also Mystacinidae, later).
The form of the lateral maxilloincisive
suture may change during ontogeny. In
D
Fig. 3. Relative length of the nasoincisive
suture in megachiropteran bats (not to scale). The
suture is long in Notopteris (A), of intermediate
length in Pteropus (B), and a point contact in
Cynopterus (C). In Nyctimene (D), the nasal and
premaxilla do not contact each other (interincisive
suture absent). Line drawings modified from
Andersen (1912). Scale = 5 mm. Abbreviation:
naisu nasoincisive suture.
6 AMERICAN MUSEUM NOVITATES NO. 3585
interincisive suture (Andersen, 1912). Based
on Andersen (1912), Romagnoli and Springer
(2000) used variation in this suture in a phylo¬
genetic context, defining a character with three
states: left and right premaxillae not in
contact; left and right premaxillae in simple
contact anteriorly; left and right premaxillae
firmly and solidly ankylosed at early age.
Giannini and Simmons (2005: character 78)
noted that the variation in the interincisive
suture among pteropodids may be better
accommodated in four character states: the
right and left premaxillary bodies may be
widely separated, in this case always accom¬
panied by a medial reduction in the thickness
of body (e.g., Eonycteris major); the bodies
may also be in close contact but not sutured
(e.g., Dobsonia); or the bodies may be in close
contact but sutured (e.g., Rousettus); or,
finally, the bodies may be fused to each other
in fully adult individuals (e.g., Nyctimene).
Another character used by Andersen (1912)
in his systematic review of megachiropterans is
the depth of the body. The body may be thin,
Fig. 4. Acerodon celebensis AMNH 153135, barely holding the alveoli of upper incisors, if
lateral view of the anterior rostrum indicating (a) present (e.g., Megaloglossus); intermediate in
angle in the lateral aspect of the maxilloincisive
depth, as in most megabats (e.g., Rousettus)',
suture and (b) notch in the ventrolateral aspect of
or very deep, as in Nyctimene and Megaerops
the same suture. Scale = 1 mm. Abbreviation: C
upper canine. ecaudatus (Giannini and Simmons, 2005:
character 79).
A more controversial character is the so-
juveniles of all megachiropteran species, the called proclivity of rostrum—a trait that
nasal process articulates with the maxilla via involves the premaxilla (see previous treat¬
a foliate suture (sensu Evans, 1993), but ments of this character in Andersen [1912],
this articulation fuses without a trace in Springer et al. [1995], and Romagnoli and
some species toward adulthood. Fully adult Springer [2000]). Proclivity of the premaxilla
individuals of Harpyionycteris, Sphaerias, can be defined with respect to the canine root.
Dyacopterus, Notopteris, Styloctenium, Neo- Two conditions are present in megachiropter¬
pteryx, and Pteralopex, as well as old speci¬ ans (Giannini and Simmons, 2005: character
mens of certain species of Pteropus, show 80). The anterior edge of the premaxilla may be
premaxillary-maxillary fusion on a regular located at the level of the anterior canine root
basis (Giannini and Simmons, 2005: character or surpassing it only slightly—up to the width
84). In one case study (Pteropus lylei; Giannini of an upper incisor (the orthoclivous condition;
et al., 2006), the maxilloincisive suture is e.g., Cynopterus, fig. 3C), or the anterior edge
among the last joints to be lost in a lifelong of the premaxilla may project anteriorly much
sequence of bone fusion that ends in a skull farther than the width of an upper incisor (the
devoid of distinguishable articulations among proclivous condition; e.g., Pteropus, fig. 3B;
elements (other than the obvious exceptions of Acerodon, fig. 4). Aproteles lacks upper inci¬
the cranial synovia, the temporomandibular sors, but its premaxilla projects only slightly
and atlanto-occipital joints). beyond the canine root, which corresponds to
The character most commonly cited with the first condition. Under this definition of
respect to the premaxillary body involves the premaxillary proclivity, Harpy ionycteris (a
2007 GIANNINI AND SIMMONS: CHIROPTERAN PREMAXILLA 7
Fig. 5. Casinycteris argynnis AMNH 48751,
oblique rostrolateral view of the rostrum showing
the dorsomedial process of the premaxilla (dmp).
Scale = 1 mm.
species typically described as having a procli-
vous rostrum) shows an orthoclivous premax¬
illa. Only the incisors are proclivous in
Harpyionycteris, and strongly so, but the pre¬
maxilla itself is not with respect to the canines.
The maxilloincisive suture takes two forms
Fig. 6. Taphozous mauritianus AMNH 257150,
in megachiropterans (Giannini and Simmons,
dorsal view of the rostrum showing the twisted
2005: character 85). The most frequent condi¬ medial edge of the premaxilla (a) and the proximal
tion is a joint at the level of the canine root, in pad-like expansion (b) typical of the premaxilla of
which an anterior projection of the maxilla some emballonurids. Scale = 1 mm.
reaches the premaxilla bridging the gap
between the canine and the second upper right premaxillary bodies are widely separat¬
incisor (e.g., fig. 3A). An alternative condition ed, so the interincisive suture is missing. The
is found in Acer o don and P ter opus, in which nasal process is thin and strongly bowed
a deep gap or vertical notch exists between laterally; in rostral view, the external nasal
the alveolar process and the canine root aperture appears rounded. In some genera
(fig. 4). Finally, the African megachiropterans (e.g., Peropteryx, Saccopteryx, Diclidurus,
Scotonycteris zenkeri and Casinycteris argyn¬ Taphozous), the dorsal end of the nasal pro¬
nis show a small, upwardly directed pro¬ cess expands into a pad-like flange that
cess located in the medioventral edge of projects medially into the external nasal
the external nasal aperture (Giannini and aperture (fig. 6; see later and Dunlop [1998]:
Simmons, 2005: character 83), termed here character 83 [part]). A less marked dorsal
the “dorsomedial process of the premaxilla”. expansion is seen in Centronycteris. Finally,
The left and right processes are in contact in the width of the nasal process is uniform
the midsagittal line (fig. 5). throughout its length in Emballonura. The
Emballonuridae: In members of this premaxilla is loosely attached to the maxilla in
family, the premaxilla lacks a palatine process. emballonurids. The usual foliate structure of
As a consequence, an incisive fissure occurs the joint (by which the intervening bones
in place of paired incisive foramina. The interlock) is not present, and the connection of
premaxillary body carries two incisors (in premaxilla and maxilla is via ligaments (a
Emballonura) or just one (in all other genera); syndesmosis).
in either case, the small incisors are frequently Dunlop (1998) used six characters of the
lost during the life of the individual. Left and premaxilla in her phylogeny of emballonurids;
AMERICAN MUSEUM NOVITATES NO. 3585
we discuss them briefly. The overall develop¬ Coleura, Rhynchonycteris, Saccopteryx, and
ment of the bone was coded in her character Peropteryx), or “2” (some or all spe¬
78, with state 0 indicating a slight reduction of cies of Saccolaimos, Mosia, Emballonura,
the bone, and state 1, a pronounced reduction Balantiopteryx, and Cormura). Again, our
“resembling bony splints” (Dunlop, 1998: 79). decision to treat different parts of the pre¬
All emballonurids were scored “1”. A problem maxilla separately conflicts with the definition
with this character definition is that the of this character proposed by Dunlop (1998).
premaxilla is taken as whole, resulting in The distal end of the premaxilla is the body,
rather ambiguous character states because and the proximal end is the dorsal end of the
components of the premaxilla can be reduced nasal process; if parts are scored separately,
to different degrees. In character 79, Dunlop different taxon-character-state associations
(1998) coded inclination of the premaxilla obtain. For instance, the outgroup Crase-
against the rostrum in two states—namely, at onycteris, the only terminal scored “3” by
an angle of 45 degrees (state 0), or “vertical Dunlop (1998), shares nothing with emballo¬
against the anterior rostrum” (state 1; these nurids under her character definition.
character states were also used by Lim However, it would share a dorsally widened
et al. [2004]: character 27, in a phyloge¬ nasal process with several emballonurids (e.g.,
netic analysis of Balantiopteryx). Three Diclidurus), as well as a widened body with
genera, Rhynchonycteris, Balantiopteryx, and other emballonurids (e.g., Emballonura alecto).
Centronycteris, were scored “1”. However, Of these states, the dorsal widening (or not) of
Dunlop (1998) did not define a horizontal the nasal process (forming the pad-like flange
reference (e.g., the rostral axis) to determine described earlier) was scored in character 29 of
the angle, so scoring a new taxon can be Lim et al. (2004: 228), defined as “premaxilla
problematic. Character 80 reflected the dorsal widens dorsally (state 0) or does not widen
development of the nasal process—or, more dorsally (state 1)”. By contrast, width varia¬
precisely, the absence/presence of a nasoincisive tion of the premaxillary body is complicated
suture. As defined by Dunlop (1998), the by other traits, such as the incisors and the
premaxillae may contact the nasals (state 0) interincisive suture, and is best expressed in
or they may not (state 1). Saccolaimos, some terms of variations on those traits (see later).
Taphozous, and some Saccopteryx were scored The premaxilla of one of the best preserved
“0”; in the remainder of emballonurids, the fossils undisputedly assigned to Emballon-
premaxilla does not reach the nasals. In uridae, the Eocene Tachypteron franzeni from
character 81, the lateral edge of the premaxilla, Messel, Germany, is well preserved in spite of
which we interpret as the lateral portion of the a largely damaged skull (see Storch et al.,
maxilloincisive suture, may be curved (state 0) 2002: fig 3a). Tachypteron resembles modern
or straight (state 1). Character 82 (also used by emballonurids in that “the premaxillae only
Lim et al. [2004]: character 28) coded the retain their nasal portion as long thin laminae
shape of the medial edge of the premaxilla, not fused to the maxillaries nor to each other”
twisted or not. Most emballonurids were (Storch et al., 2002: 192). The premaxilla
scored as having a twisted medial edge of the shows a straight profile without dorsal wid¬
premaxilla, except Balantiopteryx, Diclidurus ening or medial twisting. In general, it is more
ingens, Emballonura raffrayana, E. monticola, robust than in extant emballonurids, probably
E. furax, E. beccarii, and Mosia. Finally, because the two upper incisors are not much
Dunlop (1998) coded several conditions of reduced.
the premaxillary width in her character 83. Rhinopomatidae: As in Emballonuridae,
The premaxilla may widen distally (state 0) or the premaxilla in Rhinopoma (e.g., R. hard-
proximally (state 1); it may be of uniform wickei AMNH 219722) lacks a palatine pro¬
width (state 2); or it may widen both distally cess and has an incisive fissure rather than
and proximally (state 3). Different emballo¬ paired incisive foramina. The premaxillary
nurids were scored “0” (e.g., some species body is deep and relatively flat; in rostral
of Saccolaimos and Emballonura), or view, the body and the curved nasal process
“1” (e.g., species of Diclidurus, Cyttarops, are lyre-shaped, and the external nasal
2007 GIANNINI AND SIMMONS: CHIROPTERAN PREMAXILLA 9
Fig. 7. Rhinopoma hardwickei AMNH 208125,
digital rendering constructed from CT-scan images,
rostral view of the rostrum showing the premaxilla
and the external nasal aperture. Scale = 1 mm.
Fig. 8. Craseonycteris thonglogyai USNM
aperture appears as an inverted teardrop 528306, digital rendering constructed from CT-scan
(fig. 7). The body bears a single upper images, dorsal view of the skull, with accompanying
incisor—the second, which marks a subtle line drawing. The fused left and right medial
jugum (i.e., a relief on the rostral surface of palatine flanges are marked (*). Scale = 1 mm.
Abbreviations: C upper canine; c lower canine; il
the body caused by the underlying tooth).
first lower incisor; i2 second lower incisor; 12
This incisor inserts obliquely on the side of
second upper incisor.
the body so that the body appears edentulous
medially. The left and right bodies barely species Craseonycteris thonglongyai Hill, 1974,
contact each other at the interincisive suture in a family of its own. The left and right
and remain loosely joined by ligaments. The palatine processes are solidly ankylosed and
nasal process is bowed laterally and decreases reduced to a short, tapering spine that reaches
its width dorsally (fig. 7), tapering to a blunt less than half the distance from the pre¬
point that makes contact with the greatly maxillary body to the anterior edge of the
inflated maxillary sinuses but does not reach maxilla, the latter being deeply emarginated
the nasals. (fig. 8). Accordingly, the incisive foramina are
Craseonycteridae: Little can be added to partly coalesced, forming an incisive fissure.
the descriptions of Hill (1974: figs. 3-4) and The left and right bodies of the premaxillae
Hill and Smith (1981: fig. 1). The unique are as deep as the length of the incisors, and
structure of the premaxilla provided charac¬ the ventral edge of the external nasal aperture
ters that justified the segregation of the single is concave. A notch partially separates the left
10 AMERICAN MUSEUM NOVITATES NO. 3585
and right bodies. The left and right nasal
processes are slender, expanding dorsally
where they fuse to each other to form
a rectangular bridge over the external nasal
aperture, rostral to the shortened anterior end
of the nasals. The rim of the external nasal
aperture is thus entirely formed by the
premaxillae, which show no trace of a suture
at their dorsal point of contact. The pre¬
maxilla is loosely attached to the rostrum via
ligaments. The shape and attachment of the
premaxilla are thought to play a role in
supporting the peculiar dermal narial pad
distinctive of Craseonycteris (Hill, 1974).
Megadermatidae: This group of five ex¬
tant species in four genera has often been
described as lacking a premaxilla (since at
least Miller [1907]). Koopman (1994: 50),
when listing the characteristics of the family
Megadermatidae, included the “loss of palatal
branch of premaxillary and loss or great
reduction of its nasal branch”. Upper incisors
are lacking in megadermatids, an absence
correlated with reduction of the premaxilla.
Close examination of carefully preserved
specimens reveals that Cardioderma cor shows
a thin splint of bone that corresponds to
a nasal process, with a small ventral expansion
that represents a greatly reduced but un¬
doubtedly present premaxillary body (fig. 9).
The palatine process is entirely lacking in
Cardioderma (fig. 9). Our examination of the
other four species of megadermatids failed to
Fig. 9. Cardioderma cor AMNH 184336, ob¬
detect any trace of ossified premaxillary
lique view of the rostrum showing reduced pre¬
elements. We could not attribute this to poor maxilla. Scale = 1 mm. Abbreviations: bp body of
specimen conservation in all cases, as many of premaxilla; C upper canine; if incisive fissure; nap
the specimens available to us were very well nasal process of the premaxilla.
prepared. Accordingly, we conclude that pre¬
maxillary elements are entirely absent in medial flange. The left and right palatine
Lavia, Macroderma, and Megaderma. CT- processes are in close medial contact along
scanned images of Lavia frons AMNH 49384 their length.
further confirm this observation. The incisive foramina are of particular
Hipposideridae: Members of this family interest. A common mammalian condition,
(see also Rhinolophidae, later) lack the nasal present in many bats (but see Noctilionidae),
process of the premaxilla and have the body is that the incisive foramen (or fissure) is limited
and palatine processes widely separated from rostrally, medially, and laterally by the pre¬
the maxilla laterally, so the narrow premaxilla maxilla and caudally by the maxilla (fig. 1). In
attaches to the maxilla only via a restricted some species of Hipposideros (e.g., H. gigas),
caudal joint (fig. 10). The body forms a shal¬ the incisive foramina are completely embedded
low bar that supports the small incisors and is in the substance of the palatine process, which
continued caudally in the well-developed surrounds the foramina posteriorly as well as
palatine process that consists only of its anteriorly, medially, and laterally (Hand and