Ontogenetic and phylogenetic transformations of the lacrimal-conducting apparatus among Microchiroptera

Mamm. biol. 67 (2002) 338±357 ã Urban & Fischer Verlag http://www.urbanfischer.de/journals/mammbiol

Mammalian Biology Zeitschrift fuÈr SaÈugetierkunde

Original investigation

Ontogenetic and phylogenetic transformations of the lacrimal-conducting apparatus among Microchiroptera By LUMINITA GÚBBEL Department of Anatomy and Cell Biology, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany Receipt of Ms. 18. 09. 2001 Acceptance of Ms. 21. 05. 2002

Abstract Although there have been several reports on the structures of the lacrimal apparatus of the Chiroptera, there has been very little discussion about its morphological diversity and potential phylogenetic implications. Histological sections were used to document the anatomy of the lacrimal-conducting apparatus (LCA) in representatives of 44 chiropteran genera, including, for the first time members of Taphozous, Nycteris, Macroderma, Lavia, Hipposideros, Lonchophylla, Noctilio, Pteronotus, and Furipterus. To reconstruct the evolutionary history of the bat LCA, the distributions of the LCA features were mapped, using the computer program MacClade, onto the phylogenetic tree of SIMMONS and GEISLER (1998). The lacrimal-conducting apparatus in the Chiroptera ground plan, characterized by a well-developed nasolacrimal duct and a narial nasolacrimal duct opening, is very similar to other eutherians. Nevertheless, several evolutionary transformations have taken place within the Microchiroptera: The nycterids and noctilionoids (phyllostomids + (mormoopids + noctilionids)) are characterized by apomorphic reduction of the LCA. However, there seems to be no correlation between the absence of the LCA and the life style of these bat groups. In rhinopomatids, rhinolophids and some megadermatids, the nasolacrimal duct is truncated, opening in a ventromedial recess of the inferior nasal meatus close to the entrance of the nasopalatine duct and the vomeronasal organ. Similarly, among Nataloids (e. g., Natalus and Thyroptera), the nasolacrimal duct is shorter and opens into the inferior nasal meatus, but it has no connection to the nasopalatine duct. In emballonurids, in which the vomeronasal organ is absent, the nasolacrimal duct opens into the nasopalatine duct (e. g., Taphozous, Saccolaimus) or very close to its nasal entrance (e. g., Coleura, Cormura, Rhynchonycteris). Key words: Microchiroptera, nasolacrimal duct, nasopalatine duct, ontogeny, phylogeny

Introduction The mammalian lacrimal apparatus consists of two components, the eyeball glands (e. g., the lacrimal glands, the glands of the nictitating membrane, and the Harderian 1616-5047/02/67/06-338 $ 15.00/0.

gland), whose secretory ducts open into the conjunctival space, and the conducting components (e. g., the lacrimal canaliculi, the lacrimal sac and the nasolacrimal duct),

Nasolacrimal duct among Microchiroptera

Fig. 1. Diagrammatic representation of the lacrimal apparatus, nasopalatine duct and the vomeronasal organ in mammals.

which functionally serve the drainage of the lacrimal fluids from the orbit to the nasal floor of the nostrils, delivering its fluids to the external nostrils and to the rhinarium (Fig. 1). The function of eyeball gland secretion is generally considered to be protection and lubrication of the cornea. The lacrimal secretions are only secondarily collected by the lacrimal-conducting apparatus (LCA) and drained to the nasal cavity and the nostrils. Recent investigations have demonstrated that the eyeball gland secretions may also be involved in functions at the rostral end of the nasolacrimal duct including immune responses, photoreception, pheromone production, thermoregulation, osmoregulation, and vomeroolfaction (for reviews see Sakai 1981, 1989, 1992; Payne 1994). Among mammals, there is no direct communication between the nasolacrimal duct and the vomeronasal organ; consequently the orbital fluids (e. g., Harderian gland secretions) are not implicated in mammalian vomeronasal sensory function (Hillenius 2000; Hillenius and Rehorek 2001). However, most knowledge about the mammalian lacrimal apparatus is derived from studies of rodents, and relatively little information has been available concerning its anatomical variation in other mammalian orders. Typically, the mammalian lacrimal canaliculi join a lacrimal sac and a nasolacrimal duct before entering the lacrimal foramen. The

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nasolacrimal duct follows a characteristic course between the maxilla and the lateral wall of the nasal capsule; it emerges from the lacrimal canal at the level of the palatine bone, and changes direction abruptly at the nasolacrimal duct flexure. Near the cartilaginous anterior cupula, the duct leaves the lacrimal canal via the lateral division of the narial fenestra and joins the epithelium of the nasal sac in the area of external nostrils (ªprimaryº opening according to Starck 1960). Variations on the general mammalian pattern of the conducting components of the lacrimal apparatus occur in aquatic (e. g., the cetaceans Phocaena phocaena, Balaenoptera borealis and Lagenorhynchus albirostris, the sirenians Trichechus manatus and Dugong dugong, and the phocid Mirounga leonina) (de Burlet 1913 a, b, 1914 a, b; Matthes 1912, 1921; Kummer and Neiss 1957) and sometimes semiaquatic (e. g., the tenrecids Potamogale and Micropotamogale, and the hippopotamid Hippopotamus) (Starck 1982; Asher 2000) eutherians, in which the lacrimal-conducting apparatus is greatly reduced. In primates (e. g., Tarsius, Papio, Pan, Homo) (Reinhard 1958; Starck 1960; Maier 1997), microchiropterans (e. g., Rhinolophus, Plecotus) (Grosser 1902; Sitt 1943; GoÈbbel 1998) and perhaps some artiodactyls (e. g., Sus) (Sturm 1937) the nasolacrimal duct is truncated, opening in the inferior nasal meatus and beneath the inferior nasal concha (ªsecondaryº opening according to Starck 1960). Of these, the primates and the microchiropterans also show various transformations of the vomeronasal organ and of the nasal floor elements (e. g., Bhatnagar 1980; Bhatnagar et al. 1982; Bhatnagar and Meisami 1998; Cooper and Bhatnagar 1976; Wible and Bhatnagar 1996; Maier 1997; GoÈbbel 1998). Nevertheless, a reconstruction of the LCA in the Microchiroptera ground plan is missing, particularly caused by the lack of relevant data on many microchiropteran taxa. The variation of the LCA and the potential relationship between it and the transformation of the vomeronasal organ, have not yet been explored. As no

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comparative work on the LCA has been published to date, interspecific and interfamilial differences in the morphology of the LCA need to be documented. Because much of the information available on chiropteran LCA is incomplete, the present study was undertaken with the goals (1) to investigate the morphology of the LCA in different taxa, and (2) to survey the taxonomic distribution and the evolutionary history of the LCA in Microchiroptera.

Material and methods The present study is based on investigation of samples of Taphozous, Nycteris, Macroderma, Lavia, Hipposideros, Noctilio, Pteronotus, Lonchophylla, and Furipterus (see Tab. 1). All specimens are from the American Museum of Natural

History (AMNH), New York. The decalcified heads of these specimens were embedded in paraffin or celloidin and serially sectioned (10± 30 mm) at the Institut fuÈr Spezielle Zoologie of the University of TuÈbingen. The sections were stained with Azan. Drawings from histological sections were made with a Zeiss SV 11 microscope equipped with a camera lucida. A Zeiss D-7082 Axiophot photomicroscope and a Nikon digital camera were used for documentation. Final retouching was performed either with the airbrush technique and/or digitally with AdobePhotoshop 5.0 software. Data from other microchiropterans (see detailed lists of the specimens in GoÈbbel 1998, 2000, 2002) as well as published descriptions were taken into account. 63 species from 44 genera representing 14 families of the 18 extant families recognized by Simmons (1998) and Simmons and Geisler (1998) were included in comparisons and the discussion. All extant bat families are represented in this sample, with the exception of Craseonycteridae, Mystacinidae, Antrozoidae, and Myzopodidae.

Table 1. Microchiropteran species examined. CRL = Crown-rump length; F = frontal. All specimens were borrowed from Department of Mammalogy, American Museum of Natural History (AMNH), New York, USA and sectioned in the Institut fuÈr Spezielle Zoologie of the University of TuÈbingen, Germany. Taxa

Specimen No.

CRL, mm

Embedding

Section thickness mm

Stain

Emballonuridae Taphozous megalopogon

AMNH 257741

53

celloidin

30/F

Azan (Heidenhain)

Nycteridae Nycterus thebaica

AMNH 245212

39

celloidin

30/F

Azan (Domagk)

Megadermatidae Macroderma gigas Lavia frons

AMNH 236545 AMNH 01889

68 29

celloidin paraffin

30/F 15/F

Azan (Heidenhain) Azan (Domagk)

Rhinolophidae Hipposiderinae Hipposideros diadema

AMNH 269947

39

paraffin

15/F

Azan (Domagk)

Noctilionidae Noctilio albiventris Noctilio leporinus

AMNH 268349 AMNH 268350

31 15

paraffin paraffin

15/F 10/F

Azan (Domagk) Azan (Domagk)

AMNH 268348 AMNH 265946

23 30

paraffin paraffin

10/F 15/F

Azan (Domagk) Azan (Domagk)

AMNH 266109 AMNH 268336

15 14

paraffin paraffin

10/F 10/F

Azan (Domagk) Azan (Domagk)

AMNH 265975 AMNH 265978

17.5 24

paraffin paraffin

10/F 15/F

Azan (Domagk) Azan (Domagk)

Mormoopidae Pteronotus parnellii Phyllostomidae Lonchophylla thomasi Furipteridae Furipterus horrens

Nasolacrimal duct among Microchiroptera The recent history of the chiropteran systematic is controversial (for a historical review, see Simmons and Geisler 1998; Simmons 2000). Most systematists agree that Microchiroptera is monophyletic, and morphological data strongly support this conclusion (see the review in Simmons 2000). Simmons (1998) summarized a large data set of morphological and rDNA restriction sites, using these data to construct a new higher-level phylogeny for extant Chiroptera. These data sets were subsequently modified and expanded by Simmons and Geisler (1998), who additionally included fossils in their analysis. Both analyses found that Microchiroptera is monophyletic (Simmons 1998; Simmons and Geisler 1998). Paraphyly of Microchiroptera, with rhinopomatids and rhinolophoids or emballonurids more closely related to megachiropterans, has been supported by recent DNA studies (Hutcheon et al. 1998; Teeling et al. 2000; Springer et al. 2001; Teeling et al. 2002; Liu et al. 2001). Hutcheon et al. (1998) addressed the problem of the discrepancy between molecular and morphological data and suggested that high levels of adenine and thymine in rhinolophoids and megachiropterans may be responsible for the alliance of these taxa in the DNA studies. However, the present author follows Simmons' (1998) and Simmons and Geisler's (1998) summaries of morphological, paleontological and rDNA restriction site data and accept the monophyly of Microchiroptera a priori. Characters of potential phylogenetic significance were scored following methods described by Simmons (1993). Character transformations were evaluated by ontogenetic and outgroup comparisons, and the postulated character states were mapped onto the phylogenetic tree of Simmons and Geisler (1998). Character optimizations were calculated using the computer program MacClade version 3.0 (Maddison and Maddison 1992) and the ACCTRAN (accelerated transformation optimization) and DELTRAN (delayed transformation optimization) algorithms: ACCTRAN favours reversal over parallelism and thus generates explanations that do not refute the initial hypothesis of homology, whereas DELTRAN favours parallelism over reversals and thus generates explanations that interpret derived characters as nonhomologous synapomorphies. According to Simmons (1998, 2000) Chiroptera is assumed to be monophyletic. The terms Yinochiroptera and Yangochiroptera have been taken from Koopman (1984). The Yinochiroptera as defined by Koopman (1984, 1994) also includes the Emballonuridae. In this study, the author follows Simmons (1998) and Simmons and Geisler (1998) in recognizing two monophyletic infraorders (Yinochiroptera without Emballonuridae and Yango-

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chiroptera) and seven superfamilies: Emballonuroidea (Emballonuridae), Rhinopomatoidea (Rhinopomatidae + Craseonycteridae), Rhinolophoidea (Nycteridae + Megadermatidae + Rhinolophidae), Noctilionoidea (Noctilionidae + Nataloidea (Myzopodidae + Thyropteridae + Furipteridae + Natalidae), Molossoidea (Molossidae + Antrozoidae), and Vespertilionoidea (Vespertilionidae) within Microchiroptera. In the character analysis, multiple outgroups were included to establish character polarities (Maddison et al. 1984). Dermoptera and Scandentia have been proposed as appropriate outgroups for investigating patterns of morphological character evolution in bats (Simmons and Geisler 1998). Accordingly, comparisons were focussed on the ontogenetic series of Cynocephalus (Mielenz unpubl.) and Tupaia (Zeller 1983).

Results and discussion Morphology and taxonomic distribution of the LCA among Microchiroptera Emballonuridae This tropical family includes 13 genera (Coleura, Emballonura, Mosia, Saccolaimus, and Taphozous, and a variety of Neotropical genera, including Balantiopteryx, Centronycteris, Cormura, Cytarops, Diclidurus, Peropteryx, Rhynchonycteris, and Saccopteyx) (Koopman 1994). It is frequently regarded as the sister taxon to all other Mi-

Fig. 2. Diagrammatic representation of the lacrimal apparatus, nasopalatine duct and vomeronasal organ in Taphozous.

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Fig. 3. Taphozous longimanus (CRL: 28 mm). A. Frontal section (12-3-6) through the nasal region showing the rostral end of the nasolacrimal duct. Note the absence of the nasal opening of the nasolacrimal duct. B. Frontal section (14-3-2) through the nasal region showing the location of the entrance of the nasopalatine duct (npdo) in the maxillary recess (mxr). A represents a plane more anterior than B. ´ 22. Abbreviations for this and for all other figures: ane: apertura nasi externa; atl: anterior transversal lamina; ca: caninus; cna: cupula nasi anterior; cp: palatine cartilage; ds-nld: distal segment of nasolacrimal duct; eth I: ethmoturbinal I; inm: inferior nasal meatus; inm-r: recess of inferior nasal meatus; ip: incisive papilla; la: lacrimal; lc: lacrimal canaliculi; lca: lacrimal conducting apparatus; lf: lacrimal foramen; ls: lacrimal sac; max: maxilla; mig: multicellular intraepithelial glands; mxr: maxillary recess; mxt: maxilloturbinal; na: nasal; nc: nasal cavity; nld: nasolacrimal duct; nldo: nasolacrimal duct opening; npd: nasopalatine duct; npdc: nasopalatine duct cartilage; npdo: nasopalatine duct opening; ns: nasal septum; ob: outer bar; pas: processus alaris superior; pc: processus cupularis; pl-fn: pars lacrimalis of fenestra narina; psc: paraseptal cartilage; v: vomer; vnc: vomeronasal cartilage; vnd: vomeronasal duct; vno: vomeronasal organ.

crochiroptera (Simmons 1998; Simmons and Geisler 1998), and as such, it is expected that the emballonurids have retained several characters which could be regarded as plesiomorphic features of the Microchiroptera. With regard to the LCA in the emballonurid bat Taphozous nudiventris (T. mediven-

tris), Zuckerkandl (1910) presumed that there had to be an anatomical association between the nasolacrimal duct and the nasopalatine duct, although he could not observe it: ¹Ich bedauere, daû an dem von mir untersuchten Taphozous in der Schnittserie nur die NasenhoÈhle enthalten war, so daû nicht festgestellt werden konnte,

Nasolacrimal duct among Microchiroptera ob nicht etwa wie z. B. bei Typhlops eine Beziehung zum TraÈnenapparat besteht.ª My investigation of two specimens of Taphozous confirmed Zuckerkandl's (1910) supposition (Fig. 2). In both species of Taphozous, the nasolacrimal duct begins with two lacrimal canaliculi and the lacrimal sac at the anteromedial corner of the conjunctival space. The prenatal specimen of Taphozous longimanus already shows the condition with associated nasolacrimal and nasopalatine ducts (Figs. 3 A, B). In this fetal specimen, no opening could be detected. In an adult specimen of Taphozous melanopogon, the nasolacrimal duct opens widely (opening diameter over 980 mm) into the nasopalatine duct (Fig. 5 A); a distal, cystic segment of the nasolacrimal duct is still present (Fig. 6 A). Bhatnagar (1980) reported the correlation between the nasopalatine duct and the nasolacrimal duct for Saccolaimus saccolaimus (Taphozous saccolaimus). In all other known emballonurids (e. g., Balantiopteryx io, Coleura afra, Cormura brevirostris, Rhynchonycteris naso), the nasolacrimal duct opens near the nasal opening of the nasopalatine duct (Bhatnagar 1980; GoÈbbel 1998) (Figs. 4 A, B). However, it is worth pointing out that this condition is correlated with the fact that in most of these specimens the nasopalatine duct is very large, extending posteriorly into the area of the maxillary recess (e. g., Taphozous, see Figs. 1, 3 B). The only report of a vomeronasal organ in an emballonurid is that of Bhatnagar (1980), who indicated that Balantiopteryx io has a rudimentary (without neuroepithelium) vomeronasal organ. Examination of the five additional emballonurid genera (see specimen lists in GoÈbbel 1998, 2000) revealed no vomeronasal organ. On the basis of these observations it seems unlikely that the lacrimal fluid components have any role in vomeronasal sensory function. Typically, three distinctive histological regions of the nasolacrimal duct are described: A proximal or orbital region with stratified tall columnar epithelium, a middle region with stratified low columnar epithelium and a distal or vestibular re-

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gion with stratified squamous epithelium (Korad and Joshi 1992). In Taphozous and other emballonurids studied so far, the orbital part of the nasolacrimal duct is wide and lined with stratified epithelium which contains mucus-secreting (goblet) cells. In Rhynchonycteris naso, the nasolacrimal duct itself has glandular characteristics. Interestingly, the cystic blind distal segment of the nasolacrimal duct is still present in adults of Taphozous melanopogon and Saccolaimus saccolaimus, but it was lost in fetal specimens of Coleura afra, Cormura brevirostris, and Rhynchonycteris naso. Yinochiroptera The Yinochiroptera sensu Simmons (1998, 2000) is an Old World group comprising two superfamilies: The Rhinopomatoidea that includes only two families, the Rhinopomatidae and Craseonycteridae (each of which is monogeneric) and the Rhinolophoidea with three families, the Nycteridae, Megadermatidae and the Rhinolophidae. Examination of all histologically prepared specimens representing rhinopomatids, megadermatids, and rhinolophids suggests the presence of an LCA. In contrast, the specimens of Nycteris thebaica lack any trace of LCA. Nycterids also lack a vomeronasal organ and a nasopalatine duct. A ªsecondaryº opening of the nasolacrimal duct among yinochiropterans was first reported by Grosser (1902) for two species of the Rhinolophus (Rhinolophus ferrumequinum and Rhinolophus hipposideros). Subsequently, Sitt (1943) reported the same condition in Rhinolophus rouxii and GoÈbbel (1998) in Rhinolophus mehelyi. However, none of these authors had addressed the topographical association between the nasolacrimal duct, the nasopalatine duct, and the vomeronasal organ. The morphological variations in the relationship of these structures will be briefly discussed below. As described in rhinopomatids (Cooper and Bhatnagar 1976; Bhatnagar 1980; GoÈbbel 1998), in all investigated rhinolophids and most megadermatids, the mucosa of the inferior nasal meatus projects beneath the

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Fig. 4. Rhynchonycteris naso (CRL: 11 mm). Drawing of two frontal sections (A: section 5±2-1; B: section 5±5-4) through the nasal region at the level of the opening of the nasolacrimal duct. A. The nasolacrimal duct opening (nldo) is associated anteriorly with the nasal entrance of the nasopalatine duct (npdo). B. The nasolacrimal duct opening lies in the inferior nasal meatus beneath the maxilloturbinal (mxt). Note the presence of the multicellular intraepithelial glands (mig) in the epithelium of the nasolacrimal duct. A represents a plane more anterior than B. ´ 31.

c Fig. 5. Frontal sections of the right nasal floor of A) Taphozous megalopogon, B) Rhinopoma hardwickei (CRL: 31 mm) and C) Hipposideros diadema (CRL: 39 mm) showing the apomorphic conditions of the opening of the nasolacrimal duct. In Taphozous, the nasolacrimal duct opens into the nasopalatine duct while it is associated with the nasal entrance of the nasopalatine duct and the vomeronasal duct opening in Hipposideros and Rhinopoma, respectively. ´ 100.

Nasolacrimal duct among Microchiroptera

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lower margin of the cartilaginous nasal paries forming a ventromedial recess (Figs. 5 B, C; 6 B, C). In all these bats, the long nasopalatine duct may travel over a great distance horizontally opening into this recess of the inferior nasal meatus (Figs. 6 B, C). In prenatal stages of Rhinopoma hardwickei, the nasolacrimal duct is associated with the nasopalatine duct but ends blindly. The opening of the nasolacrimal duct into the nasal cavity develops mostly during the perinatal phases of the ontogeny. In the juvenile specimen of Rhinopoma hardwickei, the nasolacrimal duct closely approaches the epithelium of the ventromedial recess of the inferior nasal meatus and opens at its junction with the vomeronasal duct and the nasopalatine duct (Fig. 5 B, 6 B). In Megaderma lyra, Macroderma gigas, and Hipposideros diadema (Figs. 5 C, 6 C), the route of the nasolacrimal duct approximates the condition found in Rhinopoma. Nevertheless, the specimens of Megaderma and Macroderma lack a distal cystic segment of the nasolacrimal duct. Among other known yinochiropterans, the opening of the nasolacrimal duct lies in front of (e. g., Lavia frons) or behind (e. g., in all examined species of Rhinolophus) but near the entrance of the nasopalatine duct. As in emballonurids, the vomeronasal organ is either rudimentary (without neuroepithelium) (e. g., Rhinopoma, Megaderma, Macroderma, Rhinolophus, Hipposideros) or absent (Lavia, Nycteris) (Cooper and Bhatnagar 1976; Bhatnagar 1980; Wible and Bhatnagar 1996). Consideration of the yinochiropteran specimens examined thus far suggests that some of the morphological differences in the lacrimal-conducting apparatus, e. g., the presence of a distal cystic segment of the nasolacrimal duct in fetal specimens of Lavia, Rhinolophus, and Hipposideros, or absence of the nasolacrimal duct opening in fetal specimens of Rhinopoma may be a function of the developmental stage of the individual. Among Rhinolophus and Rhinopoma, however, a vestigial distal segment of the nasolacrimal duct is present even in the postnatal stages.

Yangochiroptera The infraorder Yangochiroptera includes four superfamilies: Noctilionoids with Noctilionidae + Mormoopidae + Phyllostomidae (and perhaps Mystacinidae), Nataloidea comprising Myzopodidae + Thyropteridae + Furipteridae + Natalidae, Molossoidea with Antrozoidae + Molossidae, and the monotypic Vespertilionoidea (Vespertilionidae) (Simmons and Geisler 1998; Simmons 2000). Among noctilionoids, the LCA is either totally absent (e. g., Pteronotus parnellii, Pteronotus personatus, Noctilio albiventris, Noctilio leporinus and most examined phyllostomids) or only present in an orbital cystic form (e. g., Desmodus rotundus, Artibeus jamaicensis) (Bhatnagar and Kallen 1974; GoÈbbel 1998). However, when a cystic rudimentary nasolacrimal duct is present in some of these species, it has no morphological connection to the nasal floor components (Fig. 6 D). In contrast, the members of these three families exhibit extremely different states for the vomeronasal organ and nasopalatine duct: most phyllostomids and Pteronotus parnellii have a vomeronasal organ with neuroepithelium, however, in specimens of Pteronotus parnellii, the nasopalatine duct has been lost entirely (Wible and Bhatnagar 1996). In Mormoops megalophylla, and Brachyphylla cavernarum, the vomeronasal organ is rudimentary and the nasopalatine duct present, but both fail to form in Noctilio leporinus (Wible and Bhatnagar 1996). Pteronotus personatus lacks the vomeronasal organ, but its nasopalatine duct is present (Wible and Bhatnagar 1996). Finally, Noctilio albiventris has a rudimentary vomeronasal organ and lacks a nasopalatine duct. In the three nataloids studied thus far (e. g., Thyroptera tricolor, Furipterus horrens, Natalus tumidirostris), the nasolacrimal duct also connects the mucosa of the inferior nasal meatus beneath the inferior nasal concha (ªsecondaryº opening sensu Starck 1960). There seems to be some morphological variation when the relationship among the nasolacrimal duct, nasopalatine duct, and the vomeronasal duct is considered.

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Fig. 6. Diagrams representing variation of the location of the nasolacrimal duct opening relative to the nasal entrance of the nasopalatine duct and the vomeronasal duct opening among Microchiroptera. Anterior is to left. Not to scale.

The specimens of Thyroptera lack a nasopalatine duct, but possess a rudimentary vomeronasal organ, however, the nasolacrimal duct opening has no connection to the vomeronasal duct (Wible and Bhatnagar 1996). A ªsecondaryº opening of the nasolacrimal duct and no association with the nasopalatine duct also characterize the specimens of Natalus. The specimens of Furipterus have a funnel-shaped nasopalatine duct, but the nasolacrimal duct opening lies very close to its nasal entrance. Unlike thyropterids, the natalids and furipterids lack a vomeronasal organ entirely. Among vespertilionids, only Plecotus auritus has been reported to have a ªsecondaryº nasolacrimal duct opening (Grosser 1902). My previous examination of vespertilionid specimens representing Myotis myotis, Epte-

sicus fuscus, and Miniopterus sp. and molossids (e. g., Chaerephon pumila, Molossus molossus, Molossops temminckii) revealed the presence of a well-developed LCA, which opens in the floor of the external nostrils (ªprimaryº opening). Similarly, representatives of other vespertilionids (e. g., Eptesicus serotinus, Miniopterus schreibersi, Nyctalus noctula, Pipistrellus pipistrellus, Scotophilus kuhlii, Vespertilio murinus, Myotis capaccinii, Myotis lucifugus, Myotis mystacinus) were also found to have a ªprimaryº opening of the nasolacrimal duct (Figs 7 A, B). Interestingly, the occurrence of a well-developed vomeronasal organ is a feature that may be limited to Miniopterus within vespertilionids (Fig. 7 C) (Fawcett 1919). As in rhinopomatids, rhinolophids, and some

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Fig. 7. A. Schematic frontal section through the nasal region along the plane XY (in B) showing the narial location of the nasolacrimal duct opening (ªprimaryº opening sensu STARCK 1960) in Miniopterus schreibersi. B. Reconstruction of the cartilaginous nasal capsule of a fetal Miniopterus schreibersi (CRL: 17 mm) (redrawn from FAWCETT, 1919). The membrane bones of the left side have been omitted to show the cartilaginous structures, the LCA, and the elements of the nasal floor. The mucosa of the inferior nasal meatus (inm) projects beneath the lower margin of the lateral wall and forms a ventromedial recess (inm-r). C. The nasolacrimal duct, and the nasal floor elements of the same specimens in lateral view (box in B). The mucosa of the recess of inferior nasal meatus (white dotted line) is removed to show the vomeronasal cartilage (vnc), the vomeronasal organ (vno), vomeronasal duct (vnd), and the nasopalatine duct (npd). Anterior is to left. Not to scale.

Nasolacrimal duct among Microchiroptera megadermatids, the mucosa of the inferior nasal meatus also possesses a medioventral recess for the entrance of the nasopalatine and the vomeronasal duct (Figs. 7 B, C). Nevertheless, the pattern of the LCA (Figs. 7 A, B) appears different from that seen in most yinochiropterans, in which the nasolacrimal duct connects to the nasopalatine duct. Megachiroptera The examined specimens of the Megachiroptera (e. g., Epomophorus labiatus, Rousettus aegyptiacus, Rousettus leschenaulti, Rousettus amplexicaudatus) have a well-developed LCA with a long nasolacrimal duct, which opens in the floor of the nostrils (ªprimaryº opening sensu Starck 1960) (Starck 1943; Jurgens 1963; GoÈbbel 1998). The megachiropteran nasopalatine duct is present, but the vomeronasal organ is lacking. Outgroups The specimens of Tupaia and Cynocephalus have a well-developed LCA with a nasolacrimal duct that connects the nasal cavity further rostrad from the entrance of the nasopalatine duct and that of the vomeronasal duct (ªprimaryº opening sensu Starck 1960) (Zeller 1983; Mielenz unpub.) (Figs. 8 A, B). Origin and transformation of the microchiropteran LCA The pattern of distribution of the degree of formation of LCA and the site of opening of the nasolacrimal duct, as well as its association with the nasal floor components as mapped on Simmons and Geisler's (1998) ªtotal evidenceº tree, indicate that the character state of the last common ancestor of all microchiropterans is equivocal (there are two alternative optimizations). The state with a nasolacrimal duct which opens near the entrance of the nasopalatine and/or vomeronasal duct either evolved once in the last common ancestor of all microchiropterans, as a microchiropteran autapomorphy

349

(Fig. 9 A) (ACCTRAN), or independently several times, in the last common ancestor of a clade comprising Coleura + Neotropical emballonurids, the yinochiropterans, and the furipterids (Fig. 9 B) (DELTRAN). Under ACCTRAN, reversal to a ªprimaryº opening and loss of the relationship of the LCA to the nasopalatine duct occurs at least once (e. g., in the last common ancestor of the clade nataloids + vespertilionids) (Fig. 9 A). Possibly furipterids reinvented the relationship of the LCA to the nasopalatine duct. Clearly, multiple independent events of change in the site of the opening of the nasolacrimal duct favored under DELTRAN are much simpler to account for under our current biological understanding, than the scenario provided by ACCTRAN. Because the absence or a rudimentary nasolacrimal duct occurs twice, in a clade (e. g., synapomorphy of the noctilionids + mormoopids + phyllostomids) that nest well within microchiropterans, and in nycterids, the presence of the nasolacrimal duct appears to be primitive for microchiropterans. Additionally, the distal segment of the nasolacrimal duct has been reduced (in most bat species with modified nasolacrimal duct opening) independently at least four times: (1) in a clade of emballonurids (Coleura + Neotropical emballonurids), (2) among megadermatids (Macroderma + Megaderma), (3) among species of Rhinolophus, and (4) in the last common ancestor of the nataloids. Typically, the absence of the nasolacrimal duct in mammals is correlated with an aquatic (e. g., cetaceans, sirenians, and aquatic carnivores) and sometimes with a semiaquatic life (e. g., semiaquatic tenrecids (Asher 2000) and semiaquatic artiodactyls (Starck 1982) lack a nasolacrimal duct, in contrast Ornithorhynchus anatinus (Zeller 1989) possesses one; it seems that Elephas and Manis also lack it (Weber 1927). Nevertheless, the nasolacrimal duct is also absent in members of four microchiropteran families (nycterids, phyllostomids, noctilionids, and mormoopids) regardless of their life style (i. e., none are aquatic). A ªsecondaryº opening of the nasolacrimal duct

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Fig. 8. The plesiomorphic condition of the lacrimal conducting apparatus for mammals (in this study the outgroup condition). A. Lateral view of the three-dimensional model of the fetal cartilaginous nasal capsule of Tupaia belangeri (redrawn from ZELLER 1983). The membrane bones of the left side have been omitted to show the cartilaginous structures, the LCA, nasopalatine duct and the vomeronasal organ. Anterior is to left. B. Frontal section along the plane XY (in A) showing the narial location of the nasolacrimal duct opening of Tupaia belangeri (ªprimary openingº sensu STARCK 1960). Not to scale.

Nasolacrimal duct among Microchiroptera

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Table 2. Distribution of characters of the LCA among chiropteran species* Taxon Megachiroptera 1. Pteropodidae Microchiroptera Emballonuroidea 2. Emballonuridae Yinochiroptera Rhinopomatoidea 3. Rhinopomatidae Rhinolophoidea 4. Nycteridae 5. Megadermatidae 6. Rhinolophidae Rhinolophinae Hipposiderinae Yangochiroptera Noctilionoidea 7. Phyllostomidae Desmodontinae Glossophaginae Phyllostominae Stenodermatinae 8. Mormoopidae 9. Noctilionidae Nataloidea 10. Furipteridae 11. Thyropteridae 12. Natalidae Molossoidea 13. Molossidae Molossinae Vespertilionoidea 14.Vespertilionidae Vespertilioninae Myotinae Miniopterinae

LCA**

References***

(0)

5, 8, 10, 12, 16, 17

(2) (3)

2, 11, 16, 17, 18

(2)

10, 11, 16, 17, 18

(4) (2) (2) (2) (2)

11, 18 10, 11, 16, 17, 18 1, 4, 16, 17, 18 1, 4, 16, 17, 18 16, 17, 18

(4) (4) (4) (4) (4) (4) (4)

9, 10, 11, 13, 16, 17, 18 9, 10, 16, 17 16, 17 16, 17 9, 10, 11, 13 16, 17 11, 18 11, 18

(2) (1) (1)

15, 16, 17, 18 11 16, 17

(0) (0)

11, 14, 16, 17 11, 14, 16, 17

(0) (0) (0) (0)

1, 6, 7, 9, 16, 17 1, 6, 16, 17 1, 6, 7, 9, 16, 17 3, 10, 11, 15, 16, 17

*Classification follows SIMMONS and GEISLER (1998); The terms Yinochiroptera and Yangochiroptera have been taken from KOOPMAN (1984, 1994). **Degree of formation of the lacrimal conducting apparatus (LCA) and site of the opening of the nasolacrimal duct (NLD): LCA well-developed, NLD opens (0) into the floor of the nostrils (ªprimaryº opening); (1) in the middle part of the inferior nasal meatus (ªsecondaryº opening); (2) or opens into a recess of the inferior nasal meatus closely associated to the opening of the nasopalatine duct and vomeronasal tube; (3) or opens into the nasopalatine duct; (4) LCA rudimentary with DNL cystic or absent. ***References: 1, GROSSER (1902); 2, ZUCKERKANDL (1910); 3, FAWCETT (1919); 4, SITT (1943); 5, STARCK (1943); 6, KOCH (1950); 7, FRICK (1954); 8, JURGENS (1963); 9, BHATNAGAR and KALLEN (1974); 10, COOPER and BHATNAGAR (1976); 11, BHATNAGAR (1980); 12, FEHSE (unpubl.); 13, HARTMANN (unpubl.); 14, SAMPAIO (unpubl.); 15, WIBLE and BHATNAGAR (1996); 16, GÚBBEL (1998); 17, GÚBBEL (2000, 2002); 18, this study.

comparable to that of Natalus, Thyroptera, and Plecotus also occurs in some primates (e. g., Papio, Pan, Homo) and perhaps in Sus (Starck 1975) (Fig. 10). However, this opening has been acquired independently

in these forms, because other primates (e. g., prosimians) and artiodactyls (e. g., ruminants) show the condition with a ªprimaryº opening of the nasolacrimal duct (Starck 1960, 1975).

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Nasolacrimal duct among Microchiroptera

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Fig. 10. Apomorphic condition of the lacrimal conducting apparatus among mammals. Frontal section (parallel diagonal lines represent cuts) through the cartilaginous nasal capsule (stipple) at the level of the inferior nasal meatus, inferior nasal concha (= maxilloturbinal) and the nasolacrimal duct opening (ªsecondaryº opening sensu STARCK 1960) of fetal Pan troglodytes. The membrane bones (diagonal dashed lines), the lacrimal canaliculi and the nasolacrimal duct of the left side have been reconstructed as well (redrawn from STARCK 1960). Not to scale.

Among microchiropteran taxa, evolutionary transformations occur in both the orbital glands and in the destination of the orbital fluids in the nasal cavity. A lacrimal gland is universally present in the orbital region among prenatal and adult chiropterans ex-

tending from the posterior part of the orbit along its lateral side and back into the temporal region. In contrast, the Harderian gland is generally absent and the nictitans gland is either totally absent or rudimentary, that is, without secretory elements. As men-

b Fig. 9. Evolution of the lacrimal conducting apparatus inferred from optimization of the degree of formation of the nasolacrimal duct and site of its opening in the nasal cavity onto the strict consensus tree from a ªtotal evidenceº analysis (SIMMONS and GEISLER 1998). The equivocal reconstruction in the common ancestor of microchiropterans is caused by missing data (Craseonycteridae, Mystacinidae, Myzopodidae, Antrozoidae) and different interpretation in (A) ACCTRAN and (B) DELTRAN. For character states and distribution, see table 2. Character: unordered; Tree length: 57; Consistency Index: 0.56.

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tioned previously, the microchiropterans show a diversity of morphologies of the LCA. The association of the nasolacrimal opening to that of the nasopalatine duct is not present in other eutherian mammals compared here, and to my knowledge, it has not been reported in the literature. In most microchiropterans with a modified opening of the nasolacrimal duct, the nasopalatine duct becomes a component structure of the LCA which conducts the tear fluid into the oral cavity. Functional significance of the morphological association between the LCA, the nasopalatine duct and the vomeronasal organ Based on the combination of various histological properties of the orbital glands and their relationship with the LCA, various functions have been proposed for the mammalian orbital glands, including ocular lubrication, photoreception, immune response, pheromone production, behavioral thermoregulation, and osmoregulation (Payne 1994). In some mammals (e. g., rodents), it has been suggested that the major secretory proteins of the lacrimal gland play a role in olfactory communication (Ranganathan et al. 1999). However, the function of orbital glands has only been studied in rodents, and is, unfortunately, unknown in all other mammalian orders. Therefore, this hypothesis lacks corroborating experimental and biochemical data from chiropteran lacrimal glands. The relationship between the Harderian gland, the nasolacrimal duct, and the vomeronasal organ, originally observed by Broman (1920) in squamates, suggests that the secretion from the Harderian gland is important for the function of the vomeronasal organ (see Rehorek 1997). However, the observation that chiropterans lack a Harderian gland refutes this hypothesis. On the other hand, the fact that the vomeronasal organ is absent or rudimentary in all emballonurids

and yinochiropterans excludes the potential implication of any further orbital fluid in vomeronasal sensory function. Even without these differences, there is little doubt that the reptilian and chiropteran morphological association between nasolacrimal duct and nasal floor evolved independently since this LCA feature is absent in all other mammalian orders. Another suggestion dating from the research of Born (1879, 1883) is that orbital glands may function as salivary accessory glands. In tetrapod species (e. g., some squamates), where the nasolacrimal duct communicates with the choanal groove, the orbital gland secretion discharges more or less into the buccal cavity. Thus, the orbital fluids or the fluids produced by the nasolacrimal duct itself may function as either a lubricant or a source of digestive enzymes (McDowell 1969; Saint Girons 1982). Zuckerkandl (1910) concluded that the connection between the nasolacrimal duct and the nasopalatine duct in Taphozous may be analogous to the connection between the nasolacrimal duct and the choanal grooves in snakes. However, empirical data on the secretory components of the microchiropteran orbital glands does not exist and the adaptive significance of the presented morphological arrangement remains largely speculative.

Acknowledgements I wish to express my sincere thanks to Dr. W. Maier (Institut fuÈr Spezielle Zoologie, University of TuÈbingen) and Dr. N. Simmons (AMNH, Department of Mammalogy) for placing the valuable collections of developmental material in their departments at my disposal. I also acknowledge T. Fussneger and M. Meinert for technical assistance. Thanks are also due to Dr. R. Blume for photographic assistance. My gratitude goes to Dr. L. Olsson and the anonymous reviewers whose comments improved an earlier version of the manuscript.

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Zusammenfassung Ontogenetische und phylogenetische Transformationen der TraÈnenwege innerhalb der Microchiroptera Morphologische VeraÈnderungen des TraÈnenapparates im Sinne einer vollstaÈndigen RuÈckbildung des Ductus nasolacrimalis kommen bei den aquatischen und semiaquatischen Eutherien vor; auûerdem wird bei den Primaten und Microchiropteren eine spezialisierte Úffnung des Ductus nasolacrimalis in den unteren Nasengang unter dem Maxilloturbinale beschrieben. Ontogenetische vergleichende Befunde, die den urspruÈnglichen Zustand und die Merkmalstransformationen innerhalb der Microchiroptera belegen koÈnnten, sind indes in der Literatur selten. In dieser Arbeit wird deshalb die Morphologie der TraÈnenwege auf der Basis histologischer Schnittserien aÈlterer Feten und postnataler Stadien von Vertretern der Emballonuridae, Nycteridae, Megadermatidae, Rhinolophidae, Noctilionidae, Mormoopidae, Phyllostomidae und Furipteridae erstmals untersucht. Innerhalb der Microchiroptera lassen sich die MerkmalszustaÈnde des Apparatus lacrimalis von dem fuÈr Eutheria plesiomorphen Zustand eindeutig ableiten: Die Nycteridae und Noctilionoidae (Phyllostomidae + (Mormoopidae + Noctilionidae)) zeigen eine vollstaÈndige RuÈckbildung der TraÈnenwege, wobei eine direkte Beziehung zwischen der Reduktion des Ductus nasolacrimalis und der Lebensweise (aquatisch, semiaquatisch) nicht postuliert werden kann. Bei den Rhinopomatidae, Rhinolophidae, Megadermatidae liegt die Úffnung des Ductus nasolacrimalis in einem ventromedialen Recessus des unteren Nasenganges dicht neben der Úffnung des Ductus nasopalatinus und des JACOBSONschen Organs. Die Nataloidae ((Furipteridae + Natalidae) + Thyropteridae) sind ebenso mit einer spezialisierten Úffnung des Ductus nasolacrimalis ausgestattet, es besteht aber keine direkte Verbindung zwischen den TraÈnenwegen und dem Ductus nasopalatinus (Natalus, Thyroptera). Bei den meisten Emballonuridae ist das JACOBSONsche Organ vollstaÈndig reduziert und der Ductus nasolacrimalis muÈndet entweder direkt in den Ductus nasopalatinus (e. g., Taphozous, Saccolaimus) oder dicht neben der Úffnung des Ductus nasopalatinus (e. g., Coleura, Cormura, Rhynchonycteris). Innerhalb der Microchiroptera sind die morphologischen Abwandlungen der TraÈnenwege mehrfach und unabhaÈngig voneinander in paralleler Evolution entstanden.

References Asher, R. J. (2000): Phylogenetic history of tenrecs and other insectivoran mammals. Diss. Thesis, State University of New York, Stony Brook. Bhatnagar, K. P. (1980): The chiropteran vomeronasal organ: Its relevance to the phylogeny of bats. In: Proceedings Fifth International Bat Research Conference. Ed. by D. E. Wilson and A. L. Gardner. Lubbock: Texas Tech Press. Pp. 289±315. Bhatnagar, K. P.; Kallen, F. C. (1974): Morphology of the nasal cavities and associated structures in Artibeus jamaicencis and Myotis lucifugus. Am. J. Anat. 139, 167±190. Bhatnagar, K. P.; Meisami, E. (1998): Vomeronasal organ in bats and primates: extremes of structural variability and its phylogenetic implications. Micr. Res. Tech. 43, 465±475. Bhatnagar, K. P.; Matuilionis, D. H.; Breipohl, W. (1982): Fine structure of the vomeronasal

neuroepithelium of bats: comparative study. Acta Anat. 112, 158±177. Born, G. (1879): Die NasenhoÈhlen und der TraÈnennasengang der amnioten Wirbeltiere. I. Morphol. Jb. 5, 62±137. Born, G. (1883): Die NasenhoÈhlen und der TraÈnennasengang der amnioten Wirbeltiere. II. Morphol. Jb. 8, 188±232. Broman, I (1920): Das Organon vomero-nasale Jacobsoni ein Wassergeruchsorgan! Anat. Hefte 58, 137±191. Cooper, J. G.; Bhatnagar, K. P. (1976): Comparative anatomy of the vomeronasal organ complex in bats. J. Anat. 122, 571±601. De Burlet, H. M. (1913 a): Zur Entwicklungsgeschichte des WalschaÈdels. I. Ûber das Primordialcranium eines Embryos von Phocaena communis. Gegenbaurs Morphol. Jb. 45, 523± 556. De Burlet, H. M. (1913 b): Zur Entwicklungs-

356

LUMINITA GÚBBEL

geschichte des WalschaÈdels. II. Das Primordialcranium eines Embryos von Phocaena communis von 92 mm. Gegenbaurs Morphol. Jb. 47, 645±676. De Burlet, H. M. (1914 a): Zur Entwicklungsgeschichte des WalschaÈdels. III. Das Primordialcranium eines Embryo von Balaenoptera rostrata (105 mm). Gegenbaurs Morphol. Jb. 49, 119±178. De Burlet, H. M. (1914 b): Zur Entwicklungsgeschichte des WalschaÈdels. IV. Das Primordialcranium eines Embryo von Lagenorhynchus albirostris. Gegenbaurs Morphol. Jb. 49, 393±406. Fawcett, E. (1919): The primordial cranium of Miniopterus schreibersi of the 17 millimetre total length stage. J. Anat. 53, 315±350. Frick, H. (1954): Die Entwicklung und Morphologie des Chondrocraniums von Myotis Kaup. Stuttgart: Georg Thieme. GoÈbbel, L. (1998): Zur Morphogenese der Ethmoidal- und Orbitalregion der Microchiroptera. Vergleichend-anatomische Untersuchungen mit Anmerkungen zum Grundplan und zur Phylogenie der Microchiroptera. Berlin: Wissenschaft und Technik Verlag. GoÈbbel, L. (2000): The external nasal cartilages in Chiroptera: significance for intraordinal relationships. J. Mammal. Evol. 7, 167±201. GoÈbbel, L. (2002): Morphology of the external nose in Hipposideros diadema and Lavia frons with comments on its diversity and evolution among leaf-nosed Microchiroptera. Cells Tissues Organs 170, 39±60. Grosser, O. (1902): Zur Anatomie der NasenhoÈhle und des Rachens der einheimischen Chiropteren. Morphol. Jb. 29, 1±77. Hillenius, W. J. (2000): Septomaxilla of nonmammalian synapsids: soft-tissue correlates and new functional interpretation. J. Morphol. 245, 29±50. Hillenius, W. J.; Rehorek, S. J. (2001): Eyes to nose: The Harderian gland as part of the vomeronasal system. J. Morphol. 248, 240. Hutcheon, J. M.; Kirsch, J. A. W.; Pettigrew, J. D. (1998): Base-compositional biases and the bat problem. III. The question of microchiropteran monophyly. Phil. Trans. Biol. Sci. 353, 607±617. Jurgens, J. D. (1963): Contribution to the descriptive and comparative anatomy of the cranium of the cape fruit-bat Rousettus aegyptiacus leachi Smith. Ann. University Stellenbosch 38, 3±37. Koch, L. (1950): Zur Morphologie des Craniums von Scotophilus temmincki. Diss. thesis, Jo-

hann Wolfgang Goethe University, Frankfurt am Main. Koopman, K. F. (1984): A synopsis of the families of bat ± Part VII. Bat Res. News 25, 25±27. Koopman, K. F. (1994): Chiroptera: Systematics. In: Handbook of Zoology. Mammalia. Ed. by J. Niethammer, H. Schliemann, and D. Starck, Berlin: Walter de Gruyter, Vol. VIII. Korad, V. S.; Joshi, P. V. (1992): Anatomical, histological and histochemical studies of the lacrimal gland in Schneider's leaf nosed bat Hipposideros speoris (Schneider) (Rhinolophidae, Microchiroptera). J. Animal Morphol. Physiol. 39, 71±83. Kummer, B.; Neiss, S. (1957): Das Cranium eines 103 mm langen Embryos des suÈdlichen SeeElefanten (Mirounga leonina L.). Gegenbaurs Morphol. Jb. 98, 288±346. Liu, F. G.; Miyamoto, M. M.; Freire, N. P.; Ong, P. Q.; Tennant, M. R.; Young, T. S.; Gugel, K. F. (2001): Molecular and morphological supertrees for eutherian (placental) mammals. Science 291, 1786±1789. Maddison, W. P.; Maddison, D. R. (1992): MacClade: analysis of phylogeny and character evolution, Version 3.0., Sinauer Associated, Suderland, MA. Maddison, W. P.; Donoghue, M. J.; Maddison, D. R. (1984): Outgroup analysis and parsimony. Syst. Zool. 33, 83±103. Maier, W. (1997): The nasopalatine duct and the nasal floor cartilages in catarrhine primates. Z. Morphol. Anthropol. 81, 289±300. Matthes, E. (1912): Zur Entwicklung des Kopfskelettes der Sirenen. I. Regio ethmoidalis des Primordialcraniums von Manatus latirostris. Jen. Z. Naturwissen. 48, 489±514. Matthes, E. (1921): Zur Entwicklung des Kopfskelettes der Sirenen. II. Das Primordialcranium von Halicore dugong. Z. Anat. 60, 1±306. McDowell, S. B. (1969): Toxicocalamus, a new New Guinea genus of snakes of the family elapidae. J. Zool. (London) 159, 443±511. Payne, A. P. (1994): The Harderian gland: a tercentennial review. J. Anat. 185, 1±49. Ranganathan, V.; Jana, N. R.; De, P. K. (1999): Hormonal effects on hamster lacrimal gland female-specific major 20 kDa secretory protein and its immunological similarity with submandibular gland major male-specific proteins. J. Steroid Biochem. Molec. Biol. 70, 151±158. Reinhard, W. (1958): Das Cranium eines 33 mm langen Embryos des Mantelpavians, Papio hamadryas L. Z. Anat. Entwicklungsgesch. 120, 427±455.

Nasolacrimal duct among Microchiroptera Rehorek, S. J. (1997): Squamate Harderian gland: an overview. Anat. Rec. 248, 301±306. Saint Girons, H. (1982): Histologie compareÂe des glands orbitaires des lepidosauriens. Ann. Sci. Nat. Zool., Paris 94, 171±191. Sakai, T. (1981): The mammalian Harderian gland: morphology, biochemistry, function and phylogeny. Arch. Histol. Jap. 44, 299±333. Sakai, T. (1989): Major ocular glands (Harderian gland and lacrimal gland) of the Musk Shrew (Suncus murinus) with a review on the comparative anatomy and histology of the mammalian lacrimal glands. J. Morphol. 201, 39±57. Sakai, T. (1992): Comparative anatomy of the mammalian Harderian glands. In: Harderian Glands: Porphyrin Metabolism, Behavioral and Endocrine Effects. Ed. by S. M. Webb, R. A. Hoffman, M. L. Puig-Domingo and R. J. Reiter. Berlin: Springer, Pp. 7±23. Simmons, N. B. (1993): The importance of methods. Archontan phylogeny and cladistic analysis of morphological data. In: Primates and their relatives in Phylogenetic Perspective. Ed. by R.D.E. MacPhee. New York: Plenum Press. Pp. 1±61. Simmons, N. B. (1998): A reappraisal of the interfamilial relationships of bats. In: Bats: Phylogeny, Morphology, Echolocation, and Conservation Biology. Ed. by T. H. Kunz and P. A. Racey. Washington: Smithsonian Institution Press. Pp. 3±25. Simmons, N. B. (2000): Bat phylogeny: an evolutionary context for comparative studies. In: Ontogeny, Functional Ecology, and Evolution of Bats. Ed. by R.A. Adams and S.C. Pedersen. Cambridge: University Press. Pp. 9±59. Simmons, N. B.; Geisler, J. H. (1998): Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist. 235, 1±182. Sitt, W. (1943): Zur Morphologie des Primordialcraniums und des Osteocraniums eines Embryos von Rhinolophus rouxii von 15 mm Scheitel-Steiû-LaÈnge. Gegenbaurs Morphol. Jb. 88, 268±342. Springer, M. S.; Teeling, E. C.; Madsen, O.; Stanhope, M. J.; de Jong, W. W. (2001): Integrated fossil and molecular data reconstruct bat echolocation. Proc. Natl. Acad. Sci. 98, 6241±6246. Starck, D. (1943): Ein Beitrag zur Kenntnis der Morphologie und Entwicklungsgeschichte des Chiropterencraniums. Das Chondrocranium

357

von Pteropus semindus. Z. Anat. Entwicklungsgesch. 112, 588±633. Starck, D. (1960): Das Cranium eines Schimpansenfetus (Pan troglodytes, Blumenbach, 1799) von 71 mm Scheitel-Steiû-LaÈnge, nebst Bemerkungen uÈber die KoÈrperform von Schimpansenfeten. Gegenbaurs Morphol. Jb. 100, 559±647. Starck, D. (1975): The development of the chondrocranium in primates. In: Phylogeny of the Primates. A multidisciplinary approach. Ed. by W. P. Luckett and F. S. Szalay. New York, London: Plenum Press. Pp. 127±155. Starck, D. (1982): Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage. Berlin: Springer. Vol. 3. Sturm, H. (1937): Die Entwicklung des praecerebralen Nasenskeletts beim Schwein (Sus scrofa domestica) und beim Rind (Bos taurus). Z. wiss. Zool. 149, 161±220. Teeling, E. M.; Madsen, O.; Van den Bussche, A. D.; de Jong, W. W.; Stenhope, M. J.; Springer, M. S. (2000): Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proc. Natl. Acad. Sci. 99, 1431±1436. Teeling, E. M.; Scally, M.; Kao, D. J.; Romagnoli, M. L.; Springer, M. S.; Stenhope, M. J. (2000): Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403, 188±192. Weber, M. (1927): Die SaÈugetiere. Jena: Fischer. Wible, J. R.; Bhatnagar, K. P. (1996): Chiropteran vomeronasal complex and the interfamilial relationships of bats. J. Mammal. Evol. 3, 285±314. Zeller, U. (1983): Zur Ontogenese und Morphologie des Craniums von Tupaia belangeri (Tupaidae, Scandentia, Mammalia). Diss. thesis, University of GoÈttingen. Zeller, U. (1989): Die Entwicklung und Morphologie des SchaÈdels von Ornithorhynchus anatinus (Mammalia: Protoheria: Monotremata). Abh. Senckenb. Naturforsch. Ges. 545, 1±188. Zuckerkandl, E. (1910): Das Jacobsonsche Organ. Ergebnisse Anat. Entwicklungsgesch. 18, 801±843.

Author's address: Luminita GoÈbbel, Institut fuÈr Anatomie und Zellbiologie, Martin-Luther-UniversitaÈt HalleWittenberg, Groûe Steinstr. 52, D-06097 Halle (Saale), Germany (e-mail: [email protected])