Pteropodidae

In all megachiropterans, the palatine process of the premaxilla is missing altogether (Andersen, 1912). As a result, the incisive foramina coalesce in a single large opening, the incisive fissure (fig. 2; see also Giannini et al., 2006). Interspecific variation in form of the premaxilla is thus limited to the body and nasal process, which are present in all species. Interspecific variation is nevertheless substantial; Giannini and Simmons (2005) identified nine characters of the premaxilla in megabats, which are briefly discussed here.

Fig. 2.

Pteropus lylei CM 87972, ventral view of anterior palate showing incisive fissure. Scale  =  2 mm. Abbreviations: I1 first upper incisor; I2 second upper incisor; if incisive fissure; C upper canine; mxisu maxilloincisive suture; P1 first upper premolar; P3 third upper premolar; palp palatine process of maxilla; v vomer (incisive incisure); vnc ventral nasal concha or maxilloturbinate.

Several methods have been used to describe the relative width of the nasal process, which is 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 contact, 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, Pteropus 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).

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.

Fig. 4.

Acerodon celebensis AMNH 153135, lateral view of the anterior rostrum indicating (a) angle in the lateral aspect of the maxilloincisive suture and (b) notch in the ventrolateral aspect of the same suture. Scale  =  1 mm. Abbreviation: C upper canine.

The form of the lateral maxilloincisive suture may change during ontogeny. In juveniles of all megachiropteran species, the nasal process articulates with the maxilla via a foliate suture (sensu Evans, 1993), but this articulation fuses without a trace in some species toward adulthood. Fully adult individuals of Harpyionycteris, Sphaerias, Dyacopterus, Notopteris, Styloctenium, Neopteryx, and Pteralopex, as well as old specimens of certain species of Pteropus, show premaxillary-maxillary fusion on a regular basis (Giannini and Simmons, 2005: character 84). In one case study (Pteropus lylei; Giannini et al., 2006), the maxilloincisive suture is among the last joints to be lost in a lifelong sequence of bone fusion that ends in a skull devoid of distinguishable articulations among elements (other than the obvious exceptions of the cranial synovia, the temporomandibular and atlanto-occipital joints).

The character most commonly cited with respect to the premaxillary body involves the interincisive suture (Andersen, 1912). Based on Andersen (1912), Romagnoli and Springer (2000) used variation in this suture in a phylogenetic 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 accompanied 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, barely holding the alveoli of upper incisors, if present (e.g., Megaloglossus); intermediate in depth, as in most megabats (e.g., Rousettus); or very deep, as in Nyctimene and Megaerops ecaudatus (Giannini and Simmons, 2005: character 79).

A more controversial character is the so-called proclivity of rostrum—a trait that involves the premaxilla (see previous treatments of this character in Andersen [1912], Springer et al. [1995], and Romagnoli and Springer [2000]). Proclivity of the premaxilla can be defined with respect to the canine root. Two conditions are present in megachiropterans (Giannini and Simmons, 2005: character 80). The anterior edge of the premaxilla may be located at the level of the anterior canine root or surpassing it only slightly—up to the width of an upper incisor (the orthoclivous condition; e.g., Cynopterus, fig. 3C), or the anterior edge of the premaxilla may project anteriorly much farther than the width of an upper incisor (the proclivous condition; e.g., Pteropus, fig. 3B; Acerodon, fig. 4). Aproteles lacks upper incisors, but its premaxilla projects only slightly beyond the canine root, which corresponds to the first condition. Under this definition of premaxillary proclivity, Harpyionycteris (a species typically described as having a proclivous rostrum) shows an orthoclivous premaxilla. Only the incisors are proclivous in Harpyionycteris, and strongly so, but the premaxilla itself is not with respect to the canines.

The maxilloincisive suture takes two forms in megachiropterans (Giannini and Simmons, 2005: character 85). The most frequent condition is a joint at the level of the canine root, in which an anterior projection of the maxilla reaches the premaxilla bridging the gap between the canine and the second upper incisor (e.g., fig. 3A). An alternative condition is found in Acerodon and Pteropus, in which a deep gap or vertical notch exists between the alveolar process and the canine root (fig. 4). Finally, the African megachiropterans Scotonycteris zenkeri and Casinycteris argynnis show a small, upwardly directed process located in the medioventral edge of the external nasal aperture (Giannini and Simmons, 2005: character 83), termed here the “dorsomedial process of the premaxilla”. The left and right processes are in contact in the midsagittal line (fig. 5).

Fig. 5.

Casinycteris argynnis AMNH 48751, oblique rostrolateral view of the rostrum showing the dorsomedial process of the premaxilla (dmp). Scale  =  1 mm.

Emballonuridae

In members of this family, the premaxilla lacks a palatine process. As a consequence, an incisive fissure occurs in place of paired incisive foramina. The premaxillary body carries two incisors (in Emballonura) or just one (in all other genera); in either case, the small incisors are frequently lost during the life of the individual. Left and right premaxillary bodies are widely separated, so the interincisive suture is missing. The nasal process is thin and strongly bowed laterally; in rostral view, the external nasal aperture appears rounded. In some genera (e.g., Peropteryx, Saccopteryx, Diclidurus, Taphozous), the dorsal end of the nasal process expands into a pad-like flange that projects medially into the external nasal aperture (fig. 6; see later and Dunlop [1998]: character 83 [part]). A less marked dorsal expansion is seen in Centronycteris. Finally, the width of the nasal process is uniform throughout its length in Emballonura. The premaxilla is loosely attached to the maxilla in emballonurids. The usual foliate structure of the joint (by which the intervening bones interlock) is not present, and the connection of premaxilla and maxilla is via ligaments (a syndesmosis).

Fig. 6.

Taphozous mauritianus AMNH 257150, dorsal view of the rostrum showing the twisted medial edge of the premaxilla (a) and the proximal pad-like expansion (b) typical of the premaxilla of some emballonurids. Scale  =  1 mm.

Dunlop (1998) used six characters of the premaxilla in her phylogeny of emballonurids; we discuss them briefly. The overall development of the bone was coded in her character 78, with state 0 indicating a slight reduction of the bone, and state 1, a pronounced reduction “resembling bony splints” (Dunlop, 1998: 79). All emballonurids were scored “1”. A problem with this character definition is that the premaxilla is taken as whole, resulting in rather ambiguous character states because components of the premaxilla can be reduced to different degrees. In character 79, Dunlop (1998) coded inclination of the premaxilla against the rostrum in two states—namely, at an angle of 45 degrees (state 0), or “vertical against the anterior rostrum” (state 1; these character states were also used by Lim et al. [2004]: character 27, in a phylogenetic analysis of Balantiopteryx). Three genera, Rhynchonycteris, Balantiopteryx, and Centronycteris, were scored “1”. However, Dunlop (1998) did not define a horizontal reference (e.g., the rostral axis) to determine the angle, so scoring a new taxon can be problematic. Character 80 reflected the dorsal development of the nasal process—or, more precisely, the absence/presence of a nasoincisive suture. As defined by Dunlop (1998), the premaxillae may contact the nasals (state 0) or they may not (state 1). Saccolaimos, some Taphozous, and some Saccopteryx were scored “0”; in the remainder of emballonurids, the premaxilla does not reach the nasals. In character 81, the lateral edge of the premaxilla, which we interpret as the lateral portion of the maxilloincisive suture, may be curved (state 0) or straight (state 1). Character 82 (also used by Lim et al. [2004]: character 28) coded the shape of the medial edge of the premaxilla, twisted or not. Most emballonurids were scored as having a twisted medial edge of the premaxilla, except Balantiopteryx, Diclidurus ingens, Emballonura raffrayana, E. monticola, E. furax, E. beccarii, and Mosia. Finally, Dunlop (1998) coded several conditions of the premaxillary width in her character 83. The premaxilla may widen distally (state 0) or proximally (state 1); it may be of uniform width (state 2); or it may widen both distally and proximally (state 3). Different emballonurids were scored “0” (e.g., some species of Saccolaimos and Emballonura), or “1” (e.g., species of Diclidurus, Cyttarops, Coleura, Rhynchonycteris, Saccopteryx, and Peropteryx), or “2” (some or all species of Saccolaimos, Mosia, Emballonura, Balantiopteryx, and Cormura). Again, our decision to treat different parts of the premaxilla separately conflicts with the definition of this character proposed by Dunlop (1998). The distal end of the premaxilla is the body, and the proximal end is the dorsal end of the nasal process; if parts are scored separately, different taxon-character-state associations obtain. For instance, the outgroup Craseonycteris, the only terminal scored “3” by Dunlop (1998), shares nothing with emballonurids under her character definition. However, it would share a dorsally widened nasal process with several emballonurids (e.g., Diclidurus), as well as a widened body with other emballonurids (e.g., Emballonura alecto). Of these states, the dorsal widening (or not) of the nasal process (forming the pad-like flange described earlier) was scored in character 29 of Lim et al. (2004: 228), defined as “premaxilla widens dorsally (state 0) or does not widen dorsally (state 1)”. By contrast, width variation of the premaxillary body is complicated by other traits, such as the incisors and the interincisive suture, and is best expressed in terms of variations on those traits (see later).

The premaxilla of one of the best preserved fossils undisputedly assigned to Emballonuridae, the Eocene Tachypteron franzeni from Messel, Germany, is well preserved in spite of a largely damaged skull (see Storch et al., 2002: fig 3a). Tachypteron resembles modern emballonurids in that “the premaxillae only retain their nasal portion as long thin laminae not fused to the maxillaries nor to each other” (Storch et al., 2002: 192). The premaxilla shows a straight profile without dorsal widening or medial twisting. In general, it is more robust than in extant emballonurids, probably because the two upper incisors are not much reduced.

Rhinopomatidae

As in Emballonuridae, the premaxilla in Rhinopoma (e.g., R. hardwickei AMNH 219722) lacks a palatine process and has an incisive fissure rather than paired incisive foramina. The premaxillary body is deep and relatively flat; in rostral view, the body and the curved nasal process are lyre-shaped, and the external nasal aperture appears as an inverted teardrop (fig. 7). The body bears a single upper incisor—the second, which marks a subtle jugum (i.e., a relief on the rostral surface of the body caused by the underlying tooth). This incisor inserts obliquely on the side of the body so that the body appears edentulous medially. The left and right bodies barely contact each other at the interincisive suture and remain loosely joined by ligaments. The nasal process is bowed laterally and decreases its width dorsally (fig. 7), tapering to a blunt point that makes contact with the greatly inflated maxillary sinuses but does not reach the nasals.

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.

Craseonycteridae

Little can be added to the descriptions of Hill (1974: figs. 3–4) and Hill and Smith (1981: fig. 1). The unique structure of the premaxilla provided characters that justified the segregation of the single species Craseonycteris thonglongyai Hill, 1974, in a family of its own. The left and right palatine processes are solidly ankylosed and reduced to a short, tapering spine that reaches less than half the distance from the premaxillary body to the anterior edge of the maxilla, the latter being deeply emarginated (fig. 8). Accordingly, the incisive foramina are partly coalesced, forming an incisive fissure. The left and right bodies of the premaxillae are as deep as the length of the incisors, and the ventral edge of the external nasal aperture is concave. A notch partially separates the left 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 premaxilla 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).

Fig. 8.

Craseonycteris thonglogyai USNM 528306, digital rendering constructed from CT-scan images, dorsal view of the skull, with accompanying line drawing. The fused left and right medial palatine flanges are marked (*). Scale  =  1 mm. Abbreviations: C upper canine; c lower canine; i1 first lower incisor; i2 second lower incisor; I2 second upper incisor.

Megadermatidae

This group of five extant 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 undoubtedly 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 detect any trace of ossified premaxillary elements. We could not attribute this to poor specimen conservation in all cases, as many of the specimens available to us were very well prepared. Accordingly, we conclude that premaxillary elements are entirely absent in Lavia, Macroderma, and Megaderma. CT-scanned images of Lavia frons AMNH 49384 further confirm this observation.

Fig. 9.

Cardioderma cor AMNH 184336, oblique view of the rostrum showing reduced premaxilla. Scale  =  1 mm. Abbreviations: bp body of premaxilla; C upper canine; if incisive fissure; nap nasal process of the premaxilla.

Hipposideridae

Members of this family (see also Rhinolophidae, later) lack the nasal process of the premaxilla and have the body and palatine processes widely separated from the maxilla laterally, so the narrow premaxilla attaches to the maxilla only via a restricted caudal joint (fig. 10). The body forms a shallow bar that supports the small incisors and is continued caudally in the well-developed palatine process that consists only of its medial flange. The left and right palatine processes are in close medial contact along their length.

Fig. 10.

Hipposideros armiger AMNH 216949 (A, B) and Hipposideros gigas AMNH 241044 (C, D.). Dorsal (A, C) and ventral (B, D) views of the rostrum showing the premaxilla and its wide medial attachment to the hard palate (cf. Triaenops in Fig. 11). Scale  =  5 mm. Abbreviations: ifo incisive foramen; ino incisive notch.

Fig. 11.

Triaenops persicus AMNH 216287, dorsal view of the rostrum showing the premaxilla and its medial point contact with the maxilla (cf. Hipposideros in fig. 9). Note preserved soft tissue flooring the nasal cavity between the premaxilla and maxilla. Scale  =  1 mm. Abbreviations: bp body of premaxilla; C upper canine; ino incisive notch; lfpp lateral flange of palatine process of premaxilla; mfpp medial flange of palatine process of premaxilla; mxisu maxilloincisive suture (point contact).

The incisive foramina are of particular interest. A common mammalian condition, present in many bats (but see Noctilionidae), is that the incisive foramen (or fissure) is limited rostrally, medially, and laterally by the premaxilla and caudally by the maxilla (fig. 1). In some species of Hipposideros (e.g., H. gigas), the incisive foramina are completely embedded in the substance of the palatine process, which surrounds the foramina posteriorly as well as anteriorly, medially, and laterally (Hand and Kirsch, 1998: character 9). In the alternate condition, present in many Hipposideros (e.g., H. armiger) and in all species of the other hipposiderid genera, an incisive notch is present—i.e., the incisive foramen is not completely enclosed in the palatine process. A comparison of the two conditions is provided in figure 10. Hand and Kirsch (1998) found this notched condition in seven species of Hipposideros (out of 23 scored) from five different species groups (i.e., cyclops, diadema, larvatus, speori, and pratti species groups as recognized by Simmons, 2005). As a consequence of its rather scattershot distribution, this character did not contribute a single synapomorphy in Hand and Kirsch's (1998) study.

The incisive foramen or notch in hipposiderids is accompanied by a sulcus that runs along the ventral side of the palatine process. In species with embedded foramina, the sulcus is part of a canal whose caudal end opens on the dorsal side of the hard palate, whereas its rostral end opens on the ventral side of the hard palate. The contents of that canal are unknown; we speculate that such contents may be the same as those found in another bat, Pteropus (Giannini et al., 2006)—i.e., the nasopalatine duct, the septal branches of the caudal nasal nerve of V2, and no major vessel.

The articulation of the medial palatine process with the maxilla consists of a point contact in some hipposiderid genera (e.g., Aselliscus, Triaenops; fig. 11). In other genera, including Hipposideros (fig. 10), the process contacts caudally with the entire front of the rostral edge of the palatine process of the maxilla. In Rhinonicteris, a suture is evident between the medial and lateral flanges of the palatine process (the latter reduced to splints of bone), suggesting a secondary caudal closing of the incisive foramina by premaxillary tissue.

Some hipposiderids show a distinct keel, which we term the “interincisive crest”, that is formed by the medial union of laminar expansions from the left and right palatine process dorsal to the interincisive suture (fig. 12). Bogdanowicz and Owen (1998) used this trait as a binary character in a phylogenetic analysis of the family, scoring Rhinonicteris aurantius, Triaenops furculus, T. persicus, and Cloeotis percivale as having a “hornlike crest in middle of dorsal part of premaxillae” (Bogdanowicz and Owen, 1998: 38, character 1). Similarly, Hand and Kirsch (1998) used an equivalent character defined as “Premaxillae: (0) not especially thickened; (1) very thick with distinct crest on dorsal surface at line of contact” (Hand and Kirsch, 1998: 85, character 10). Hand and Kirsch (1998) identified Triaenops persicus, Rhinonicteris aurantius, and the Australian early Miocene R. tedforti and Brachipposideros nooraleebus as having state 1, but Cloeotis percivale was scored “0”. In his revision of the group, Hill (1982: 168) noted a “distinct ridge on the upper face” of the premaxillae as occurring in Rhinonicteris and Triaenops but not in Cloeotis. In our sample, we observed that in Cloeotis percivale (e.g., AMNH 168161), an interincisive crest is present. As in Triaenops (e.g., T. persicus AMNH 216237), the crest in Cloeotis is much shorter than the crest of Rhinonicteris (e.g., R. aurantius AMNH 1972113, 197216, fig. 12) but is nonetheless present.

Fig. 12.

Rhinonicteris aurantius AMNH 197216, lateral (A) and oblique rostrodorsal (B) view of the rostrum showing the interincisive crest of the premaxilla. Scale  =  1 mm. Abbreviations: C upper canine; I2 second upper incisor; iic interincisive crest.

The presence of the interincisive crest supported a clade formed by Brachipposideros and Rhinonicteris when characters were unordered in the morphological analysis of Hand and Kirsch (1998). Triaenops and two fossil genera (the Australian early Miocene Riversleigha and Xenorhinos) joined that clade if characters were ordered (Hand and Kirsch, 1998). Interestingly, the premaxilla is unknown in Riversleigha and Xenorhinos (scored “?” in Hand and Kirsch, 1998: characters 9–10). Therefore, the recovery of these fossils nested within this clade predicts the presence of an interincisive crest in these forms. Note that if Cloeotis is scored “1” for this character, the presence of the interincisive crest diagnoses a larger clade inclusive of this form plus Coelops (represented by C. frithi), in which the absence of interincisive crest would represent a reversal (see Hand and Kirsch, 1998: fig. 5.1b).

Within Hipposideros, Hill (1963: 9) described the variation in premaxillary characters as follows (our synonymy in square brackets): Considerable variation is displayed in the form of the premaxillae, which basically form a projecting structure with a V-shaped or U-shaped junction with the maxillae [ =  maxilloincisive joint, palatine part]. Considered together, they vary from a narrow oblong structure not greatly expanded posteriorly at its junction with the maxillae to a wide structure almost filling the anterior palatal emargination with a wide, sometimes fan-shaped union with the maxillae. Their lateral edges may be deeply notched so that with the maxillae they form the walls of the anterior palatal foramina [ =  incisive foramina]. In some species, delicate anterior enclosing processes [ =  lateral flange of the palatine process] are developed to form the anterior walls of these foramina: these processes in other species completely enclose the foramina which are thus contained within the premaxillae. The anterior palatal foramina in some species are small and rounded and in others are large and oval, elongate or slit-like.

Finally, two conditions of the premaxillary body are found in Hipposideros. The diastema between the single left and right incisor may be straight and flat, as in H. armiger (e.g., AMNH 216949), or a small recess may be present in the body between the incisors, as, for instance, in H. gigas (e.g., AMNH 241044; see fig. 10).

Rhinolophidae

The premaxilla in Rhinolophus is very similar to that of Hipposideros (cf. figs. 10, 13, 14). The incisive foramina (notches) are variably included in the substance of the palatine process and may open to the caudolateral side of the palatine process, as in Rhinolophus ferrumequinum nippon AMNH 245591 (fig. 13), or the incisive notches may be closed caudally by the medial convergence of lateral flanges (e.g., Rhinolophus alcyone AMNH 236298; fig. 14). The ventral sulcus seen in hipposiderids is also present in Rhinolophus (e.g., R. alcyone AMNH 269922; R. ferrumequinum AMNH 160473; R. hildebrandti AMNH 161917).

Fig. 13.

Rhinolophus ferrumequinum nippon AMNH 245591, digital rendering constructed from CT-scan images, rostrodorsolateral (A) and rostrodorsal (B) views of the skull. Scale  =  5 mm. Abbreviations: bp body of premaxilla; C upper canine; I2 second upper incisor; ino incisive notch; ppmx palatine process of premaxilla.

Fig. 14.

Rhinolophus alcyone AMNH 236298, dorsal view of the rostrum. Scale  =  1 mm. Abbreviations: a wedge-shaped gap between left and right premaxillary bodies; bp body of the premaxilla; C upper canine; I2 second upper incisor; ifo incisive foramen; lfpp lateral flange of the palatine process of the premaxilla; mfpp medial flange of the palatine process of the premaxilla; mx maxilla.

Nycteridae

As in hipposiderids and rhinolophids, in this family the nasal process of the premaxilla is entirely lacking. The nycterid premaxilla can be described as a sloping body that is continued caudally, forming a wide obtuse angle, by the roughly horizontal, laterally diverging palatine process (fig. 15). The left and right bodies are separated from the maxillae by a lateral gap, and articulate with each other via ligaments. Each body bears the alveoli for two small incisors. The body is barely deeper than the incisor roots, which are recurved dorsocaudally to accommodate their lengths in the short body. Apparently, the palatine portion of the premaxilla corresponds to the lateral palatine flange seen in other bats. This conclusion is based on the fact that the palatine laminae diverge caudolaterally from the sagittal plane, encompassing a single large incisive fissure (contra Miller, 1907). In this interpretation, Nycteris lacks the medial flange of palatine process, differing in this way from the superficially similar premaxilla of hipposiderids and rhinolophids, in which the medial flange is well developed. The premaxilla abuts the maxilla caudolaterally, forming an overlying edge to which ligaments are attached (fig. 15).

Fig. 15.

Nycteris grandis FMNH 151186, dorsal view of the rostrum. Scale  =  1 mm. Abbreviations: bp body of premaxilla; C upper canine; I1 first upper incisor; I2 second upper incisor; if incisive fissure; lfpp lateral flange of palatine process of premaxilla; mx maxilla; na nasal; palp palatine process of the maxilla.

Within nycterids, variation exists in the interincisive suture. The left and right premaxillary bodies may be in contact, as in N. grandis (e.g., FMNH 151186; fig. 15), or the bodies may be partially separated, as in N. thebaica (e.g., AMNH 213046). It is interesting to note that in the latter, the first upper incisors converge medially, even though the left and right bodies are separated, thus forming a continuous incisor row despite the separation in the supporting bones.

Mystacinidae

The premaxilla in Mystacina is complete in that it possesses a body and the palatine and nasal processes are both well developed (e.g., Mystacina robusta AMNH 160269, 214243; M. tuberculata 173919, 174825). The left and right premaxillae are fused to each other and to the maxilla. The nasal process is wide and reaches the nasals, but the nasoincisive suture is short (fused in adults). The nasal process exhibits an expansion of its rostral edge, so the processes are projected forward (fig. 16A; see also Pteropodidae). Thus, in lateral view, the external nasal aperture has the appearance of a short tube. The depth of the body varies: at the interincisive suture, the left and right bodies are relatively narrow. In spite of this, the root of the large I1 is very long and takes a divergent dorsal course, running parallel to the lateral edge of the external nasal aperture up to one half the height of the aperture (fig. 16A).

Fig. 16.

Mystacina tuberculata AMNH 173919 (A), Noctilio albiventris AMNH 243904 (B), and Pteronotus parnelli AMNH 269063 (C), digital rendering constructed from CT images, rostrolateral view of the rostrum showing the premaxilla produced as a short tube. Scale  =  1 mm.

The medial flange of the palatine process is present and separates two very small incisive foramina. An unpaired, medial accessory palatine foramen of similar size but unknown content is present rostral to the paired incisive foramina.

Noctilionidae

In Noctilio, the nasal processes of the premaxilla are wide and are fused with the nasal bones dorsally and with the rostral processes of the maxilla posterolaterally. The nasal processes are projected rostrally, as described for Mystacina, but this condition is especially well marked in Noctilio albiventris (fig. 16B). Also as in Mystacina, the root of the large I1 is divergently directed dorsally in both species of Noctilio, running parallel to the lateral edge of the external nasal aperture. Both Noctilio albiventris and N. leporinus show a notch in the premaxilla where the lower canine fits, but this notch is markedly larger in the latter (e.g., N. leporinus FMNH 58122); in addition, the small size and crowded position of I2 contributes to the large, arched diastema between I2 and C. A low ridge is present just above the diastema and I2. Noctilio albiventris lacks the ridge, and the diastema is proportionally smaller.

Adult specimens of both Noctilio species lack incisive foramina. Simmons and Conway (2001) used this trait as a phylogenetic character and cited it as a synapomorphy diagnosing Noctilionidae. The absence of patent incisive foramina of any kind makes it difficult to establish the homology of the continuous bony lamina that covers the anterior palate in Noctilio. However, an examination of juveniles (Noctilio albiventris AMNH 79651, 79673) indicates that the incisive foramina are present at early age and are separated by a thin and short medial flange of the palatine processes (fig. 17). At the stage of AMNH 79673, the maxilla already bears a crescent-shaped, rostrally oriented process that underlies the incisive foramen, termed here the “incisive process of the maxilla”. Eventually, this process closes the incisive foramen (e.g., in AMNH 79651), later fusing with the premaxilla and sealing the anterior palate. As a consequence, Noctilio possesses lateral and medial flanges of the palatine processes and lacks incisive foramen or fissure due to the growth of an anteriorly directed incisive process of the maxilla. Premaxilla and maxilla are seamlessly fused in adult specimens of Noctilio.

Fig. 17.

Noctilio albiventris AMNH 79673 (A) and AMNH 79651 (B), ventral view of the right hard palate showing the inferred process of closing the incisive foramen by the incisive process of the maxilla. Scale  =  0.5 mm. Abbreviations: C upper canine; I1 first upper incisor; I2 second upper incisor; ifo incisive foramen; ipmx incisive process of the maxilla; mfpp medial flange of the palatine process of the premaxilla; mx maxilla; mxisu maxilloinsive suture.

Mormoopidae

In most species of Pteronotus, including the Cuban fossil P. pristinus (e.g., ROM 59132; see Simmons and Conway, 2001), the premaxilla is remarkably similar to that of Mystacina in all respects (fig. 16C). Pteronotus personatus and the two species of Mormoops differ in that the rostral edges of the nasal processes are not distinctly projecting. Mormoops further differs in that the medial accessory palatine foramen is lacking (see Simmons and Conway, 2001).

Simmons and Conway (2001) used three premaxillary characters from Simmons and Geisler (1998) in their phylogenetic analysis of Mormoopidae. These characters were not informative within Mormoopidae but were used for outgroup comparisons. These characters reflected the fusion of the premaxilla to the maxilla (their character 1, state 0), the presence of the palatine process (character 2, state 0), and the presence of incisive foramina (character 3, state 0).

Phyllostomidae

Members of this family generally have the nasal process of the premaxilla fused to the maxilla and nasal and the left and right bodies fused to each other. The medial flange of the palatine process is present, so the incisive foramina are well delimited. Three aspects of the phyllostomid premaxilla are remarkable. First, the medial flange of the palatine processes may contact the maxilla in the usual way (i.e., articulating with the maxilla at the level of the palatal shelf), or the medial palatal process may instead articulate above the level of the palatine shelf, bypassing the rostral edge of the palatine process of the maxilla (fig. 18). The latter condition is found in several genera (e.g., Vampyrodes, Carollia), and in some of these (e.g., Platyrrhinus) there is a prominence of the maxilla (with a corresponding vault in the palate) that acts as a platform supporting both the vomer and the caudal edge of the medial flange of the palatine process (fig. 18).

Fig. 18.

Platyrrhinus helleri AMNH 267182, dorsal view of the rostrum. Indicated with (*) is the maxillary platform that receives both the vomer caudally and medial flange of the palatine process of the premaxilla rostrally. The presence of an accessory medial foramen is also notable. Scale  =  1 mm. Abbreviations: afo accessory medial foramen; C upper canine; I1 first upper incisor; I2 second upper incisor; ifo incisive foramen; mfpp medial flange of the palatine process of the premaxilla; v vomer (incisive incisure).

Carstens et al. (2002) scored the presence of an unnamed “third” foramen in the premaxilla of some glossophagines (their character 4, state 1), an alternative condition to the presence of just two foramina (i.e., the paired incisive foramina; their character 4, state 0). This unpaired opening (fig. 19A) corresponds to our accessory incisive foramen (see Mystacina), which is anteromedial to the paired incisive foramina. The accessory incisive foramen occurs in several phyllostomid genera, sometimes accompanied by nutrient foramina located anterior or posterior, dorsal or ventral to it—a trait that exhibits high intraspecific variation. The medial accessory foramen, present also in some other yangochiropterans (e.g., Mystacina, Pteronotus), may be the remainder of the secondary closing of a rostral wedge-shaped gap between left and right bodies (see Myzopoda). This conclusion is based on observations of some phyllostomids with weakened premaxillary bodies due to reduced dentition (e.g., Anoura caudifer CML 5493, Anoura geoffroyi AMNH 263192 [fig. 19A], Choeroniscus minor AMNH 267948 [fig. 19B]).

Fig. 19.

Anoura geoffroyi AMNH 263192 (A) and Choeroniscus minor AMNH 267948 (B), ventral view of the anterior palate showing the possible homology of the accessory medial foramen and the wedge-shaped gap caused by reduction of insicsors and the concomitant weakening of the premaxillary body. Scale  =  1 mm. Abbreviations: afo accessory medial foramen (parentheses indicates presumed homology); C upper canine; I1 first upper incisor; I2 second upper incisor; ifo incisive foramen; mfpp medial flange of the palatine process of the premaxilla.

Many phyllostomids (e.g., Carollia perspicillata AMNH 266126; see fig. 20) show the same pattern of long I1 roots penetrating high up in the lateral edge of the external nasal aperture that was noted previously in Mystacinidae and Noctilionidae. However, the reverse pattern is seen in other phyllostomids in which I2 is greater than I1 so that the I2 root is the one that penetrates vertically into the substance of the premaxilla (e.g., Anoura geoffroyi AMNH 263193).

Fig. 20.

Carollia perspillata AMNH 266126, sequence from 56 to 60 coronal CT images through the rostrum showing the dorsal penetration and divergence of the first upper incisor roots into the substance of the left and right premaxilla. Gray areas in the slices represent soft tissue. A digital rendering of the whole skull constructed from CT images in rostral view (A) is given as reference, indicating the approximate area covered by the slices (white frame). Scale  =  1 mm. Abbreviations: c lower canine; cI1 crown of first upper incisor; i lower incisors; na nasal; nac nasal cavity; rI1 root of first upper incisor.

Examination of available juvenile specimens from species representing three different subfamilies (Phyllostomus hastatus AMNH 17034 [Phyllostominae], Anoura caudifer CML 3146 [Glossophaginae], and Artibeus lituratus AMNH 76677 [Stenodermatinae]) suggests that the nasal processes are long in phyllostomids, abutting the nasals laterally and tapering to a point at the anterior third of the nasal length. Thus, the lateral side of the external nasal aperture is completely delimited by the nasal process, and the nasoincisive suture is very long, reaching well caudad to the level of the upper canine. The maxilloincisive suture may remain visible in adult specimens of some nectar-feeding bats (e.g., Scleronycteris). Other variations observed in long-nosed nectar-feeding bats (e.g., Anoura caudifer) include the presence of a depression between the upper canine jugum and the nasal process of the premaxilla and a wide I1-I1 diastema derived from reduction of the bulk of incisors.

Important shape variation occurs in relation with rostral length and shape in phyllostomids. Premaxillary proclivity is marked in some nectar-feeding taxa (e.g., Lonchophyllini), with the premaxilla accompanying the general elongation of the rostrum seen in those bats. Gregorin and Ditchfield (2005) showed an interesting increase in proclivity within Lonchophyllini, from a moderate condition in Lionycteris to an extreme case in Xeronycteris, in which proclivity is so marked that the orientation of I1 is almost horizontal with respect to the alveolar line. At the other end of the spectrum are fruit specialists in the Stenodermini, which show extreme shortening of the rostrum and caudal displacement of the external nasal aperture. For instance, Centurio exhibits a premaxilla that is orthoclivous with respect to the level of the upper canine. In Ametrida and Sphaeronycteris, the premaxilla is affected by the extreme retraction of the external nasal aperture and the upturning of the rostrum; as a consequence, the body of the premaxilla is strongly slanted dorsocaudally. Wetterer et al. (2000) contrasted this condition (their character 47, state 1) with the gently sloping rostrum of most phyllostomids (state 0), in which the nasal process of the premaxilla is not significantly inclined and lies roughly perpendicular to the palatine process. Surprisingly, seemingly opposite morphogenetic processes (extreme elongation versus retraction of the rostrum) produce a similar effect in the orientation of the premaxilla.

In another group of dietary specialists, the blood-feeding Desmodontinae (vampire bats), the premaxilla has a triangular shape in ventral view as it bears large, blade-shaped incisors that converge rostrally and are used to cut the skin of birds and mammals to obtain blood. The medial flanges of the palatine processes are very thin, and the incisive foramina are large. Also, the premaxilla is elevated with respect to the maxillary alveolar line, which effectively separates the large incisor blades from the upper canines (fig. 21).

Fig. 21.

Desmodus rotundus AMNH 248951, lateral (A) and ventral (B) view of the rostrum showing the dorsal displacement of the premaxilla with respect to the maxilla in (A) and the large size of the incisive foramina in (B). Scale  =  1 mm. Abbreviations: C upper canine; I1 first upper incisor; ifo incisive foramen; mfpp medial flange of the palatine process of the premaxilla; vnc ventral nasal concha or maxilloturbinate.

Myzopodidae

All of the premaxillary components are present in Myzopoda aurita. In adult individuals (e.g., USNM 449282), the left and right bodies decrease in height medially and are well separated by a wedge-shaped gap—a moderate “anterior palatal emargination” sensu Simmons and Geisler (1998; their character 13, state 1, and character 14, state 0; see fig. 22). The body of the premaxilla bears two incisors, with I1 being significantly smaller than I2. The alveolus of I1 is short and obliquely displaced dorsolaterally. The nasal process of the premaxilla is fused to the maxilla laterally; the relationship of this process with the nasal is not clear due to early bone fusion. The palatine process of the premaxilla is fused to the maxilla and vomer medially and is rostrally connected to the body via a thin bar of bone (fig. 22). This obliquely oriented bar closes the incisive foramen anteriorly. A relatively small, kidney-shaped incisive foramen divides the palatal process into a thick medial flange and a wide lateral flange. The left and right medial flanges converge medially in an elevated position with respect to the alveolar line, forming a platform that receives the incisive incisure of the vomer dorsally.

Fig. 22.

Myzopoda aurita AMNH 257130, rostrodorsal (A) and caudoventral (B) view of the rostrum showing the wedge-shaped gap between the incisive foramina. Scale  =  1 mm. Abbreviations: C upper canine; I1 first upper incisor; I2 second upper incisor; ifo incisive foramen; v vomer.

The precise contacts of the nasal process are unclear, as the maxilloincisive and nasoincisive sutures are seamlessly fused in the specimens available to us (AMNH 257130, USNM 449282). The same is true for other yangochiropteran groups. The rostral edge of the nasal process is straight and gently inclined dorsocaudally so the external nasal aperture is sloping.

Thyropteridae

The premaxilla in Thyroptera is likely complete and similar in most respects to the myzopodid premaxilla except for the fact that those incisive foramina are closed or, at least, greatly reduced. In T. tricolor AMNH 246236, a minute foramen is present on the left side, which possibly represents the corresponding incisive foramen of other bats like Myzopoda, whereas a right foramen is absent. An alternative interpretation of the thyropteran premaxilla is that the palatine process is absent altogether, so the rostral gap is similar to the emarginate condition seen in vespertilionids (see later). We favor the first option (palatine process present, incisive foramina obliterated) on the basis of comparisons with Myzopoda (see earlier), Furipterus, and Natalus (see later).

The rostral edge of the nasal process is gently slanted, as in Myzopoda. Sutures fuse early in the life of individuals, so the contacts of the nasal process are unclear. A precanine chamber, likely a glandular premaxillary sinus, is visible through the external nasal aperture, to which the premaxilla and probably the maxilla contribute (see Natalidae). Two bi-lobed incisors are obliquely inserted in the body; I1 is smaller than I2. The left and right bodies are separated by a wedge-shaped gap, as in Myzopoda.

Furipteridae

The premaxilla in the monotypic Furipterus is rather similar to the myzopodid premaxilla—that is, left and right bodies are well separated by a wedge-shaped gap, and the bodies connect with the medial flange of the palatine process via a thin bar. However, in Furipterus (e.g., F. horrens AMNH 265975, 267218), large incisive foramina pierce the palatine process, and upper incisors are subequal, relatively small, with a diastema separating I2 from the upper canine. The rostral shortening of the nasal creates a notch in the sloping dorsal edge of the premaxilla.

The other genus of the family, the monotypic Amorphochilus (e.g., AMNH 36261), is further modified. The left and right bodies are completely separated, apparently due to the lack of ossification of the medial flange of the palatine process. Incisive notches are large, widely open rostrally as a consequence of the absence of the thin bony bridge between the medial palatine process and the body, and separated from each other by the incisive incisure of the vomer. (It is unclear whether a reduced medial flange of the palatine process underlies the protruding vomer.)

Natalidae

The natalid premaxilla is similar to the myzopodid premaxilla in most respects, except that in natalids the premaxilla does not project as far rostrally, and the medial flange of the palatine processes is not elevated above the alveolar line. The straight lower canine fits in an arched socket formed by the diastema present between I2 and the upper canine. Early fusion precludes precise determination of the relationships of the nasal process of the premaxilla to the maxilla and nasals and makes it difficult to determine the precise location of the maxilloincisive suture. The thinness of the bone suggests that the premaxilla may participate, together with the maxilla, in a large precanine sinus (as seen in CT-scanned specimens; fig. 23; e.g., AMNH 206695). This character is shared with Thyroptera.

Fig. 23.

Natalus stramineus AMNH 206695, digital rendering constructed from CT images, lateral view of the skull. The thinness of the premaxillary bone makes visible a large precanine sinus indicated with (*). Scale  =  5 mm.

Vespertilionidae

This speciose family is remarkably uniform in premaxillary morphology. The nasal processes are fused to the maxilla in all taxa we examined. Observations of young specimens (e.g., Lasiurus intermedius AMNH 253710) indicate that the nasal processes articulate with the nasals dorsally (fig. 24). The left and right bodies are fused to the maxilla laterally at the level of the alveolar line and are separated from each other by a wide medial gap. This, together with the lack of palatine processes and the retracted anterior edge of the maxilla, contributes to the palatal emargination typical of vespertilionids (see Simmons and Geisler, 1998: characters 13–14). This emargination varies from very wide (e.g., in Nyctalus and Lasiurus, in which the emargination hollows virtually all the space between left and right tooth rows and reaches M1 caudally; fig. 25) to relatively narrow (e.g., in Harpiocephalus, in which the emargination is less wide than the space between the inner upper incisors [I1] and barely surpasses the canine caudally). The single important, variable feature that involves the body in vespertilionids is that it may bear one or two incisors.

Fig. 24.

Lasiurus intermedius AMNH 253710, line drawing of the dorsal view of the rostrum. Scale  =  1 mm. Abbreviations: bp body of premaxilla; fr frontal; if incisive fissure; mx maxilla; mxisu maxilloincisive suture; na nasal; naisu nasoincisive suture.

Fig. 25.

Lasiurus seminolus AMNH 219950, ventral view of the anterior hard palate. Scale  =  1 mm. Abbreviations: C upper canine; I2 second upper incisor.

Molossidae

The nasal process of the premaxilla is always present and is fused to the maxilla in molossids. While Cheiromeles (fig. 26B) and some Chaerephon show small paired incisive foramina and a variously developed medial flange of the palatine process, variation exists regarding the body and the palatine process in the remainder of the molossids. Molossid genera typically show “emarginate” or “non-emarginate” palates. Examples of the non-emarginate condition include Cynomops, Eumops (fig. 25A), Molossops, Molossus, Promops (New World) and Cheiromeles (fig. 26B), Myopterus, and Mops (Old World). In these forms, left and right premaxillary bodies are fused to each other, and incisive foramina may be present in the form of a single opening of varying size (e.g., in species of Eumops; fig. 26A).

Fig. 26.

Eumops perotis AMNH 248390 (A), Cheiromeles torquatus AMNH 103922 (B), and Tadarida brasiliensis AMNH 219336 (C), ventral view of palate (see the text). Scale  =  1 mm.

In molossids that have emarginate palates (e.g., Tadarida brasiliensis; fig. 26C), the left and right bodies are separated by a small gap. This space is continued caudally in a narrow fissure in Mormopterus, Nyctinomops, and Tadarida. This resembles the condition seen in vespertilionids, although in the latter the emargination is markedly wider. In Chaerephon pumilus, the left and right bodies are separated by a gap, but each one is connected by a thin bar of bone to the medial flange of the palatine process, and paired incisive foramina are present (see Bouchard, 1998: fig. 2). However, in other species (e.g., C. chapini) the rostral gap is nearly closed, and the incisive foramina are minute (see Fenton and Eger, 2002: fig. 2), and yet in C. ansorgei the palatine process is not ossified (see Bouchard, 2001: fig. 2). In Tomopeas ravus (e.g., LSU 25072, 25084), formerly included in Vespertilionidae and transferred to Molossidae by Sudman et al. (1994; see also Simmons, 1998; Simmons and Geisler, 1998; and Gunnell and Simmons, 2005), the morphology of the premaxilla is as in typical vespertilionids.

In view of these morphologies, it is possible that the non-emarginate condition, with a single or no incisive opening, may represent a gradual secondary closing of an emarginate palate, as seen in vespertilionids and Tomopeas—successive sister groups to crown-group molossids (Simmons, 1998; Simmons and Geisler, 1998), as well as in Tadarida and related genera. That is, it is possible that the single palatine opening in molossids (e.g., in Eumops) would be primarily homologous to the medial accessory palatine foramen in other yangochiropterans (e.g., phyllostomids). This hypothesis can be tested with the histological study of the contents of the accessory palatine foramen.

Eocene Bats

Simmons and Geisler (1998) described the basic structure of the premaxilla in the four best-known Eocene fossil genera of bats: Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx. All of these taxa have a premaxilla with a well-developed nasal process that articulates with the maxilla via sutures. No notch is present between the premaxilla and maxilla anterior to the upper canine. In Hassianycteris, the only taxon known from multiple skulls preserved in lateral view, the nasoincisive suture is of intermediate length, and the premaxilla does not widen dorsally (Smith and Storch, 1981). There is no evidence of twisting of the medial edge of the premaxilla in any of the four Eocene genera.

The body of the premaxilla is clearly present and bears two incisors on each side of the jaw in Archaeonycteris, Hassianycteris, and Palaeochiropteryx (Simmons and Gesisler, 1998). The premaxilla appears to be orthoclivous in Hassianycteris (Smith and Storch, 1981); the degree of proclivity is unclear in the remaining Eocene genera.

Simmons and Geisler (1998) were unable to determine whether the palatine process was present or absent in Archaeonycteris, Hassianycteris, and Palaeochiropteryx. However, Smith and Storch (1981: 158, 164) noted that Hassianycteris has a premaxilla in which “the palatal branch is not well developed; and the premaxillaries, although possibly in contact on the midline, do not appear to have been fused.” They further noted that “the apparent shape and reduction of the premaxillary is quite reminiscent of the derived condition of this cranial element in emballonurids.”

The number of upper incisors in Icaronycteris could not be determined unambiguously in the original description, but at least one incisor was present (Jepsen, 1966). Jepsen (1966) also noted presence of a medial diastema between the upper incisors in Icaronycteris, but it was not clear whether this was an artifact of preservation of the holotype. The palatine process was thought to be present in Icaronycteris (Simmons and Geisler, 1998), but details of morphology (e.g., presence or absence of medial and lateral flanges) could not be determined, because the lower jaws obscured the palate on all available specimens. A new specimen of Icaronycteris (AMNH 125000), in which the palate is exposed, clearly confirms the presence of a palatine process with a medial flange fully separating left and right incisive foramina, as well as a medial diastema between upper incisors (fig. 27). It also suggests that the adult number of upper incisors is two.

Fig. 27.

Icaronycteris sp. AMNH 125000, ventral view of palate. Scale  =  1 mm. Abbreviations: C upper canine; I1 first upper incisor; I2 second upper incisor; ifo incisive foramen; ppmx palatine process of premaxilla.