Introduction
The ethmoidal region of the mammalian skull reveals a significant
contribution to the understanding of mammalian ontogeny, evolution,
phylogeny, and functional anatomy (e.g. Paulli, 1900a, b, c; Voit, 1909;
Reinbach, 1952a, b; Kuhn, 1971; Kuhn and Zeller, 1987; Maier, 1991, 1993a;
Craven et al., 2007, 2010; Macrini, 2012; Ruf, 2014; Ruf et al., 2014). Being
part of the chondrocranium it is completely cartilaginous in early
ontogenetic stages. The cavum nasi inside is anteriorly limited by the cupula
nasi anterior, dorsally by the tectum nasi and lamina cribrosa, laterally by
the paries nasi, posteriorly by the cupula nasi posterior, and ventrally by
the solum nasi (lamina transversalis anterior, paraseptal cartilages, and
lamina transversalis posterior). The paries nasi of the pars lateralis and
pars posterior gives rise to most of the olfactory turbinals and is therefore
also called paries conchalis. The septum nasi divides the nasal cavity in
symmetrical halves and separates the paraseptal spaces. During postnatal
ontogeny the cartilaginous ethmoidal structures undergo a significant
transformation caused by degeneration, ossification and replacement: the
cupula nasi anterior and adjacent structures as well as parts of the
paraseptal cartilages remain cartilaginous; the turbinals become completely
ossified except for the marginoturbinal, atrioturbinal, and in certain
species the anterior portions of the maxillo- and nasoturbinal; the tectum
nasi, paries nasi, and parts of the paraseptal cartilages become resorbed and
replaced by dermal bones (e.g. Voit, 1909; Reinbach, 1952a, b; Zeller,
1987).
The nasal cavity of mammals is unique in housing a distinct number of complex
conchae that are supported by bony lamellae, the turbinals (or turbinates)
and has the two-fold function of thermoregulation and olfaction (Paulli,
1900a, b, c; Hillenius, 1992; Kemp, 2006). The oldest known ossified remnants
of turbinals are described in the advanced non-mammaliaform cynodont
Brasilitherium riograndensis and can be dated back into the Late
Triassic (Ruf et al., 2014). The anteriormost turbinals (in particular the
maxilloturbinal, anterior portion of nasoturbinal) and in many species the
anterior process of the first ethmoturbinal are covered by respiratory
epithelium for warming and moistening the inspired air whereas the posterior
turbinals (frontoturbinals, ethmoturbinals, interturbinals), the semicircular
crista or lamina as well as the posterodorsal part of the nasal septum are
covered by olfactory epithelium that carries the olfactory receptors of the
first cranial nerve; the distribution of the olfactory epithelium differs
among species and depends on their macrosmatic level (Le Gros Clark, 1951;
Ruf, 2004; Rowe et al., 2005; Smith et al., 2007, 2014a; Eiting et al., 2014;
Van Valkenburgh et al., 2014b).
For more than a century investigations of internal nasal structures, in
particular the turbinals, were based on histological serial sections and
therefore restricted to prenatal and early postnatal stages due to technical
limitations. During this period a tremendous number of excellent
morphological descriptions were published that cover almost all mammalian
orders as well as some other amniote taxa (e.g. Gaupp, 1900; Voit, 1909; de
Beer, 1929; Reinbach, 1952a, b; Starck, 1960; Maier, 1980; Kuhn, 1971; Ruf,
2004). Most of these works focused on comparative descriptions and were
mostly restricted to one or a few species. Though they provide significant
contributions to the understanding of the early ontogeny of the mammalian
nose and detecting general homologies, in many cases the incorporation of
adult characters was not possible (Maier, 1993a). However, this is due to the
fact that in postnatal ontogeny the turbinal pattern may change significantly
by ossification, outgrowth of additional small lamellae on the turbinals
(so-called epiturbinals), and additional interturbinals (e.g. Ruf, 2014).
Only very few publications have dealt with juvenile or adult crania in this early
stage of research on ethmoidal anatomy. The most important one may be the
work of Paulli (1900a, b, c), who investigated the adult turbinal and nasal
sinus pattern in about 100 species covering several mammalian orders.
However, he introduced a different nomenclature (ectoturbinals,
endoturbinals) simply by numbering the turbinals and without any
consideration of ontogenetic origin, topography, and evolution of the
structures, which clearly hinders detecting homologies among different species
(see Ruf, 2014, for more details).
Thanks to modern non-invasive imaging techniques, e.g. high-resolution
computed tomography (µCT), research on the ethmoidal region has
changed dramatically in recent years. Adult specimens can now be investigated
to elucidate the three-dimensional architecture of the internal nasal
structures (e.g. Clifford and Witmer, 2004; Rowe et al., 2005; Van
Valkenburgh et al., 2004, 2011; Craven et al., 2007, 2010; Macrini, 2012;
Maier and Ruf, 2014; Ruf, 2014). A recently published supplement to
The Anatomical Record is an outcome of a symposium dealing with the vertebrate
nose that took place at the 10th International Congress of Vertebrate
Morphology in Barcelona in 2013 and demonstrates the renaissance of research
on the ethmoidal region especially in primates (see Van Valkenburgh et al.,
2014a). However, comprehensive comparative studies of the prenatal to adult
turbinal skeleton of the putative sister group of primates, the Scandentia
(tree shrews), to elucidate ontogenetic transformations, systematic
relationships, and evolutionary scenarios are still missing.
Based on recent morphological and phylogenetic studies the order Scandentia
comprises two families: Tupaiidae (Tupaia, Dendrogale,
Urogale, Anathana) and the monospecific Ptilocercidae
(Ptilocercus lowii, pen-tailed tree shrew) (Helgen, 2005).
Previously both families were classified as subfamilies within Tupaiidae
(Wilson, 1993; McKenna and Bell, 1997). Ptilocercus holds a key
position as it might resemble the basal clade within extant Scandentia
representing the scandentian ancestral morphotype in many respects apart from
several autapomorphic unique features (Olson et al., 2004; Sargis, 2007;
Wible, 2009; Roberts et al., 2011).
Scandentia are nested within the major placental clade Euarchontoglires.
While Rodentia and Lagomorpha are distinct sister groups forming the cohort
Glires, the sister-group relationships among the remaining three orders
(Dermoptera, Scandentia, Primates) are still discussed based on molecular
data (Murphy et al., 2001; Springer et al., 2003; Nishihara et al., 2006;
Bininda-Emonds et al., 2007). According to Meredith et al. (2011), a
molecular supertree analysis combined with relaxed molecular clocks,
Scandentia are the sister group of Glires. A recent study of O'Leary et
al. (2013) is based on morphological and palaeontological data and clearly
supports the sister-group relationship of Scandentia and Dermoptera to form
the clade Sundatheria. However and although the phylogenetic position of
Scandentia is still under discussion, this taxon is still essential for
understanding cranial anatomy, evolutionary transformations, and systematics
not only of Primates but also of the entire euarchontogliran clade.
Anatomy and development of Scandentia has been investigated mainly in
Tupaia but also in Ptilocercus lowii in regard of skeletal
and soft tissue anatomy, craniogenesis, embryogenesis, and placentation
(e.g. Lyon Jr., 1913; Le Gros Clark, 1925, 1926; Spatz, 1964; Kuhn and
Schwaier, 1973; Zeller, 1983, 1986a, b; Kuhn and Liebherr, 1988; Wible and
Zeller, 1994; Funke and Kuhn, 1998; Wible, 2009, 2011). Ontogeny of internal
nasal structures is only known from Tupaia belangeri (Zeller, 1983,
1987), Tupaia glis (Spatz, 1964), and Tupaia javanica
(Henckel, 1928; Spatz, 1964). A detailed PhD thesis of the chondrocranium of
a fetal Ptilocercus including the ethmoidal region was conducted by
Janßen (1993). The adult internal rostrum pattern of Ptilocercus
has been investigated by LeGros Clark (1926) and Wible (2011). However, due
to the application of an inappropriate terminology (see comment below),
certain misinterpretations of the turbinal skeleton arose in both
publications. Furthermore, the investigation of Wible (2011) is solely based
on macroscopic preparation of the nasal cavity, which hinders a detailed
understanding of the three-dimensional arrangement of the turbinal skeleton
in many respects.
Three-dimensional plate model of the cranium of the fetal
Ptilocercus lowii (30 mm CRL): (a) dorsal view,
(b) right lateral view. Reconstruction of dermal bones is restricted
to left side. Cartilage is drawn in blue, dermal bones in yellow, and
endochondral bone in grey. Abbreviations: al, alisphenoid; ao, ala orbitalis;
boc, basioccipital; bs, basisphenoid; cM, cartilago Meckeli; can, cupula
nasi anterior; cnp, cupula nasi posterior; co, commissura orbitonasalis; cp,
cartilago paraseptalis; de, dentary; eoc, exoccipital; fai, foramen acusticum
internum; fm, foramen magnum; fo, foramen opticum; fon, fissura
orbitonasalis; fr, frontal; hy, hyoid; in, incus; ipar, interparietal; ju,
jugal; la, lacrimal; lar, larynx; lc, lamina cribrosa; lic, lamina
infracribrosa; lpc, limbus praecribrosus; ma, malleus; mx, maxilla; na, nasal; oc, otic capsule; ors,
orbitosphenoid; par, parietal; pas, processus alaris superior; pim, pila
metoptica; pip, pila praeoptica; pmx,
premaxilla; pn, paries nasi; prz, processus zygomaticus; ps,
presphenoid; soc,
supraoccipital; sq, squamosal; tn, tectum nasi; vo, vomer. Scale bars equal
2 mm.
Here we provide the first description of an ontogenetic transformation of the
nasal cavity from fetal to adult stage in Ptilocercus lowii. The
adult pattern is compared to an adult Tupaia sp. whose turbinal
skeleton has been briefly mentioned in Ruf (2014). Significantly different
character patterns in early ontogenetic stages of the already investigated
Tupaia species are considered based on literature (see above).
However, we should point out that differences in size and shape may be
affected by heterochronic growth in the respective species of Tupaia
and therefore should not be overestimated. Finally, our results are an
important contribution to cranial anatomy and ontogeny of Euarchontoglires
and help to elucidate the primate ancestral morphotype.
Three-dimensional plate models of the right fetal nasal
capsule of (a) Ptilocercus lowii (30 mm CRL) and
(b) Tupaia belangeri (34 days) in medial view (b).
Abbreviations: at, atrioturbinal; can, cupula nasi anterior; cnp, cupula nasi
posterior; co, commissura orbitonasalis; dnl, ductus nasolacrimalis; et I,
II, III, ethmoturbinal I, II, III; ft 1, frontoturbinal 1; lc, lamina
cribrosa; lic, lamina infracribrosa; lpc, limbus praecribrosus; ls, lamina
semicircularis; lta, lamina transversalis anterior; ltp, lamina transversalis
posterior; mat, marginoturbinal; mt, maxilloturbinal; nt, nasoturbinal; pa,
pars anterior; pas, processus alaris superior; pp, pars posterior; pru,
processus uncinatus; tn, tectum nasi. Scale bars equal 2 mm.
Material and methods
In order to elucidate the prenatal ontogeny an embryo of Ptilocercus lowii (no. Ib, 30 mm CRL, 17.7 mm HL) from the Hubrecht Collection,
Utrecht (the Netherlands), and currently located at the Museum für
Naturkunde zu Berlin (Germany) was investigated by histological serial
sections. These sections (10 µm) were used to create a
three-dimensional plate model according to Born (1883, modified according to
Zeller, 1983) (Figs. 1, 2); for details see Janßen (1993). Drawings of
selected slices have been prepared based on enlarged photomicrographs
(Figs. 5, 6). In addition, histological serial sections of several dated
fetal stages of Tupaia belangeri from the Hans-Jürg Kuhn
collection (Göttingen, Germany), now part of the Senckenberg collection
(Frankfurt am Main, Germany) and currently located at Medizinische
Fakultät Universität Münster (Germany), were investigated for
comparison (see Zeller, 1983, 1987, for details). The focus was on a
34-day-old fetus. In addition, data from Spatz (1964) on a neonate
Tupaia glis were also used for comparison. As all these
Tupaia specimens have been imported from Bangkok and the
Tupaia belangeri–chinensis group is very closely
related to Tupaia glis, it is likely that all specimens represent
the same species (see Zeller, 1983, for further details, Wible, 2011).
An adult specimen of Ptilocercus lowii (ZMB 3992) from the
collection of the Museum für Naturkunde zu Berlin (Germany) was
investigated with the local µCT scanner nanotom (GE
phoenix|x-ray); voxel size (resolution) is
0.01991 mm × 0.018991 mm × 0.018991 mm. In addition the
cleaned skull of an adult Tupaia sp. (collection W. Maier,
Tübingen) was scanned with the µCT device v|tome|x s (GE
phoenix|x-ray) housed in the Steinmann-Institut für Geologie,
Mineralogie und Paläontologie, Universität Bonn, Germany; voxel size
is 0.05865 mm × 0.05865 mm × 0.05865 mm. Virtual
three-dimensional reconstructions of the turbinal skeleton were made with the
software Avizo 7.1 (FEI) (Figs. 3, 4).
Virtual three-dimensional models of the adult rostrum of
(a, c, e) Ptilocercus lowii (ZMB 3992)
and (b, d, f) Tupaia sp. (collection
W. Maier): (a) and (b) left lateral view, (c) and
(d) dorsal view, (e) and (f) ventral view. Skull
bones are made translucent to allow view on reconstructed turbinal skeleton
highlighted in the same colour code as in Fig. 4. Scale bars equal 5 mm.
Due to the fact that µCT scans reveal predominantly hard tissues of
the body, the present study refers to ossified skeletal structures of the
ethmoidal region (Figs. 7–15). However, a detailed description of the
cranial soft tissue and cartilaginous structures in a Ptilocercus
fetus is presented in Janßen (1993).
Terminology
The anatomical terminology was used according to Voit (1909),
Reinbach (1952a, b), and Ruf (2014). Most recent investigations (e.g. Wible,
2011) are still based on the terminology mainly introduced by Paulli (1900a,
b, c) in which turbinals are simply numbered and divided into ectoturbinals
(fronto- and interturbinals) and endoturbinals (ethmoturbinals and
erroneously the lamina semicircularis). Thus, non-homologous structures and
those with different ontogenetic origin are consequently homologized which is
a limiting factor for the comparison of turbinal patterns among investigated
species (Ruf, 2014). This problem is mainly raised by the lack of knowledge
of prenatal and early postnatal ontogeny of internal nasal structures in most
species.
The terminology of frontoturbinals used in the present work is different from
Spatz (1964), Zeller (1983, 1987), and Janßen (1993) as the homology
especially of frontoturbinals is still problematic. Therefore, here we use
the developmental pattern (Kuhn and Zeller, 1987) to define the specific
frontoturbinals because topographic criteria are insufficient due to
ontogenetic variations.
Comparative description
The ethmoidal region of the Ptilocercus fetus is still completely
cartilaginous and resembles approximately the same developmental stage as a
38-day-old fetus of Tupaia belangeri (Zeller, 1983, 1987).
Extension and expansion of nasal cavity
Head length and cranial length of the investigated Ptilocercus fetus
are 17.7 and 16.0 mm, respectively (Fig. 1). The length of the nasal capsule
is 7.7 mm, its maximum width 5.0 mm and its maximum height 2.3 mm. Length,
height, and width of the nasal capsule amount to 5.9, 5.1, and 2.6 mm in a
fetal Tupaia belangeri (34 days), and 8.3, 5.2, and 3.1 mm in a
neonate Tupaia glis. In order to detect the length of the nasal
capsule relative to the entire skull length the ratio of basicranial length
posterior of the cupula nasi posterior to ethmoidal region was calculated.
This ratio is 1 : 1.2 in Ptilocercus and 1 : 0.9 in both
Tupaia specimens. Thus the prenatal nasal capsule of
Ptilocercus is longer than that of Tupaia (Fig. 2).
In the adult Ptilocercus the ethmoidal region extends posteriorly
between the orbits and reaches the level of the postorbital bar (Fig. 3a, c).
It measures 20.70 mm and the basicranium behind the nasal cavity is
14.26 mm long. Thus, the ratio is 1 : 1.45. In contrast the ethmoidal
region of Tupaia ends in the anterior third of the orbit (Fig. 3b,
d). The length of the nasal cavity of Tupaia is 25.10 mm; the
basicranium behind is 18.36 mm. Thus, the ratio of basicranium posterior to
the ethmoidal region to nasal cavity length is 1 : 1.37. Though the nasal
cavity becomes proportionally longer during postnatal growth, it still remains
shorter but wider in Tupaia (Figs. 3, 4). In contrast, in
Ptilocercus it becomes evident that the orbits narrow the posterior
nasal space (Figs. 3c, d, 4e, f, 9, 10, 11, 12).
Virtual three-dimensional models of the right adult turbinal
skeleton of (a, b, e) Ptilocercus lowii
(ZMB 3992) and (b, c, f) Tupaia sp.
(collection W. Maier): (a) and (c) medial view, (b) and
(d) lateral view, (e) and (f) ventral view.
Abbreviations: et I, II, III, ethmoturbinal I, II, III; ft 1, 2,
frontoturbinal 1, 2; it, interturbinal; ls, lamina semicircularis; mt,
maxilloturbinal; nt, nasoturbinal; pa, pars anterior; pp, pars posterior.
Scale bars equal 5 mm.
Septum nasi and septum interorbitale
In fetal stages the septum nasi is a continuous vertical lamina that connects
the cupula nasi anterior and the cupula nasi posterior. Dorsally it is fused
to the tectum nasi, ventrally it is continuous with the lamina transversalis
anterior in many species. The free ventral rim is inflated as also observed
in the investigated Scandentia (Fig. 5). In lateral view the septum nasi
resembles a triangle with its largest height just in front of the lamina
cribrosa. During postnatal ontogeny the septum nasi becomes mostly ossified
and part of the ethmoid bone in adult stages. Posteriorly its ventral edge
fuses to the vomer. The alae vomeris form lateral wings on the septum nasi.
However, the anterior portion correlated with the flexible anterior nasal
cartilages remains cartilaginous throughout the entire lifetime (see Zeller,
1983, 1987). This general fetal as well as adult pattern can also be observed
in our investigated Scandentia.
Drawings of histological cross sections through the pars anterior of
the fetal nasal cavity from anterior (a) to posterior (b)
of Ptilocercus lowii (30 mm CRL). Abbreviations: at, atrioturbinal;
cM, cartilago Meckeli; cp,
cartilago paraseptalis; de, dentary; dn, ductus nasopalatinus; dnl, ductus
nasolacrimalis; et I, ethmoturbinal I; mt, maxilloturbinal; mx, maxilla; na,
nasal; nt, nasoturbinal; pa, pars anterior; pmx, premaxilla; pn, paries nasi;
ppm, processus palatinus medialis; sn, septum nasi; st, septoturbinal; tn,
tectum nasi; vno, vomeronasal organ. Scale bars equal 2 mm.
In the pars anterior of the fetal Ptilocercus the septum nasi shows
a so-called septoturbinal, a longitudinal prominent ridge (Fig. 5b).
Anteriorly, the ossified septum nasi rises on the level of the upper second
incisor; its ventral inflation is hollowed and restricted to the pars
anterior (Fig. 7c). The septoturbinal is still present in the adult
Ptilocercus and represents a hollow longitudinal bulge on the dorsal
part of septum nasi (Fig. 7c, e). Two small and short septoturbinal-like
ridges approach the nasoturbinal from ventrally and fuse to the latter.
Neither a distinct crista galli nor a spina mesethmoidalis is present in the
investigated ontogenetic stages (Figs. 6, 10a, 11a).
Drawings of histological cross sections through the pars lateralis
and posterior of the fetal nasal cavity from anterior (a) to
posterior (b) of Ptilocercus lowii (30 mm CRL).
Abbreviations: cM, cartilago Meckeli; de, dentary; et I, II, ethmoturbinal I, II; fr, frontal; ft 1, 2,
frontoturbinal 1, 2; gm, glandula maxillaris; gnl, glandula nasi lateralis;
la, lacrimal; lc, lamina cribrosa; mx, maxilla; ob, olfactory bulb; on,
olfactory nerves; pa, pars anterior; pn, paries nasi; po, pars obtecta
(paries conchalis); pp, pars posterior; rli, recessus lateralis inferior;
rls, recessus lateralis superior; sn, septum nasi; vo, vomer. Scale bars
equal 2 mm.
In the investigated perinatal stages of Tupaia no septoturbinal is
evident though the septum nasi of a neonate Tupaia glis shows a
conspicuous thickened ridge (Spatz, 1964; Zeller, 1983, 1987). The
investigated adult specimen clearly shows a very long septoturbinal that runs
from the pars anterior far into the pars posterior and almost resembles the
pattern of Ptilocercus (Figs. 7d, f, 8b, d, 9b, 10b, 11b, 12b).
According to Spatz (1964) Tupaia javanica develops a short and low
but distinct crista galli in late prenatal ontogeny. In contrast to
Ptilocercus the septum nasi and tectum nasi of Tupaia form
a caudally oriented spine right at the anterior border of the lamina
cribrosa, the so-called spina mesethmoidalis. This spine is already very
prominent in prenatal stages (Spatz, 1964; Zeller, 1983, 1987) but fused to
the frontals and therefore not identifiable anymore.
At the posterior end of the ethmoidal region in all investigated stages of
Tupaia the septum nasi continues into a septum interorbitale that
separates the orbits (Fig. 15d). This is not the case in
Ptilocercus, which has a flat trabecular plate and
basicranium in this region (Fig. 15c).
Lamina cribrosa
The lamina cribrosa is the posterior roof of the nasal cavity. Its anterior
border is the limbus praecribrosus. Laterally the lamina cribrosa is limited
by the limbus paracribrosus and posteriorly by the limbus postcribrosus of
the lamina infracribrosa (Fig. 2). All these borders become ossified and
incorporated into the dermal bones of the osteocranium.
In the fetal Ptilocercus the lamina cribrosa is still cartilaginous
and trapeziform. Its greatest width is along the limbus praecribrosus and it
is ventrally concave (Figs. 1a, 2a, 6). This concavity is correlated with the
space needed by the bulbus olfactorius. In contrast the lamina cribrosa of a
fetal Tupaia belangeri and a neonate Tupaia glis is almost
triangular (Spatz, 1964; Zeller, 1983, 1987). The convexity of the lamina
cribrosa is not as deep as in Ptilocercus (Fig. 2b), but the depth
increases during ontogeny (Zeller, 1983, 1987). The limbus postcribrosus is
more pronounced in Ptilocercus than in Tupaia.
In the adult stages of Ptilocercus and Tupaia the concavity
is still present though restricted to the anterior part in the former
(Figs. 10a, 11–14, 15a, c).
The lamina cribrosa shows numerous foramina olfactoria that are the pathways
for the fila olfactoria (cranial nerve I). Their number increases during
ontogeny while their size decreases. This trend is also observable in the
investigated Scandentia and well documented in the ontogenetic series of
Tupaia belangeri (Zeller, 1983, 1987). In the adult Scandentia the
posterior section of the lamina cribrosa above ethmoturbinal III shows no
foramina and therefore corresponds to the lamina infracribrosa; this area
appears to be larger in Ptilocercus.
Pars anterior of nasal cavity
The anterior part of the nasal cavity houses several turbinals, most of which
are organized in a ventral row. The anteriormost turbinal, the
marginoturbinal, arises from the anterior nasal cupula and is continuous with
the atrioturbinal. All these structures persist postnatally as cartilage.
Thus, they are not visible in the µCT scan of the adult specimens
and therefore are not described here.
The maxilloturbinal of Ptilocercus continues the ventral turbinal
row as a simple medial infolding of the cartilaginous sidewall of the nasal
cavity, the so-called paries nasi (Figs. 2a, 5, 6b). In the adult the roof
and sidewalls of the cartilaginous nasal capsule no longer exist and are
functionally replaced by the dermal bones; the maxilloturbinal appears to be
completely ossified. The maxilloturbinal anterior–posterior extension is
comparable to that of the first turbinal, and both are the longest turbinals
in Ptilocercus (Fig. 4a, b). The ossified turbinal projects from the
premaxilla on the level of the first upper incisor and ends on the level of
the second upper molar on the maxilla. The base (or root) of the
maxilloturbinal curves smoothly from the sidewall of the nasal cavity to the
nasal floor in the posterior part of the nasal cavity. Anteriorly and
posteriorly the maxilloturbinal of Ptilocercus resembles a straight
lamella that projects into the nasal cavity. In between it shows a
complicated double scroll; its dorsal portion is embraced by ethmoturbinal I
(Figs. 4a, b, 7a, c, e, 8a, c, 9a).
µCT cross-section images of the pars anterior of the adult
rostrum from anterior to posterior of (a, c,e)
Ptilocercus lowii (ZMB 3992) and (b, d,
f) Tupaia sp. (collection W. Maier). Numbers in figures
refer to number of original µCT slices. Abbreviations: C – upper
canine; cnl, canalis nasolacrimalis; et I, ethmoturbinal I; I2, upper incisor
2; ls, lamina semicircularis; mt, maxilloturbinal; nt, nasoturbinal; P1, 2,
3, upper premolar 1, 2, 3; pa, pars anterior; rfr, recessus frontalis; sfm,
septum frontomaxillare;
sm, sinus maxillaris; sn, septum nasi; st, septoturbinal; vo, vomer. Scale
bars equal 2 mm.
In general the maxilloturbinal pattern of Tupaia is quite similar to
Ptilocercus (Figs. 2b, 7b, d, f, 8b). However, the adult
maxilloturbinal is proportionally shorter only about two-thirds of the total
length of the first ethmoturbinal due to the greater absolute length of the
latter (Fig. 4c, d). The maxilloturbinal starts at the level of the second
upper incisor and ends on the level of the last upper premolar. However, it
remains unclear if its anterior tip is still cartilaginous and therefore not
visible in the µCT scan. Medially the maxilloturbinal of the adult
Tupaia shows several ridges that resemble epiturbinals not present
in Ptilocercus (Figs. 4e, f, 7).
The nasoturbinal of the Ptilocercus fetus is a straight and in
cross-section short lamella projecting from the dorsal sidewall of the nasal
capsule (between tectum nasi and paries nasi) into the anterior nasal cavity
above the maxilloturbinal. Its anterior extension is identical to that of the
maxilloturbinal and caudally it fuses to the paries nasi very close to the
maxilloturbinal (Figs. 2a, 5a). The bases of both turbinals remain widely
separated.
By outgrowth the nasoturbinal pattern changes significantly in the adult
stage. The ossified nasoturbinal is supported by a ridge of the nasal bone
and starts somewhat behind the anterior tip of the maxilloturbinal as a short
anterior process (Figs. 4a, b, 7a, c). However, it remains unclear if the
anterior tip of the nasoturbinal is still cartilaginous as some soft tissue
is visible in the µCT scan. Caudally the nasoturbinal ends above
midway of the maxilloturbinal on its root (Figs. 4b, 7c). In the cross section
the nasoturbinal is an almost straight lamella that is situated above the
maxilloturbinal and never reaches the medial extension of the latter
(Fig. 7a).
In the adult Tupaia the nasoturbinal is less developed than in
Ptilocercus and resembles a quite slender lamella that appears to be
displaced ventrally along its entire length. The anterior portion rises from
the lateral border of the nasal, and posteriorly the nasoturbinal ends right
above the base of the maxilloturbinal (Figs. 4c, d, 7b, d).
The lamina semicircularis (crista semicircularis) resembles a wall separating
the border between the pars anterior and the pars lateralis. It develops as a
posterior extension of the paries nasi (Zeller, 1987) and forms a
sickle-shaped vertical but distinctly bent lamella in the fetal stage of
Ptilocercus (Fig. 2a). The lamina semicircularis shows a prominent
posteroventral processus uncinatus that supports the hiatus semilunaris.
Lamina semicircularis and nasoturbinal are separated by a large gap
(Fig. 2a).
The adult Ptilocercus shows a very similar pattern. However, the
lamina semicircularis appears to have undergone a significant growth in
height and length, and therefore it bulges out into the nasal cavity and forms
the medial wall of the anterior confluent parts of the frontoturbinal recess
and maxillary sinus (Figs. 4a, b, 7e, 8a). The lamina has a lateral
epiturbinal-like outgrowth that is oriented dorsally. This structure becomes
integrated into the swollen apical edges of the lamina's flanks above and
below the hiatus semilunaris. The processus uncinatus of the ventral flank is
still evident in the adult (Fig. 8a, c). Posteriorly, the dorsal flank
becomes a horizontal lamina that shows an apical hollowed inflation and is
continuous with the lamina cribrosa (Figs. 8c, 9a).
µCT cross-section images of the pars lateralis and
posterior of the adult rostrum from anterior to posterior of (a,
c) Ptilocercus lowii (ZMB 3992) and (b,
d) Tupaia sp. (collection W. Maier). Numbers in figures refer to
number of original µCT slices. Abbreviations: cla, canaliculus
lacrimalis; et I, II, ethmoturbinal I, II; fla, foramen lacrimale; ft 1, 2,
frontoturbinal 1, 2; it, interturbinal; ls, lamina semicircularis; M1, upper
molar 1; mt, maxilloturbinal; P2, 3, upper premolar 2, 3; pa, pars anterior;
po, pars obtecta (paries conchalis); pp, pars posterior; pru, processus
uncinatus; rfr, recessus frontalis; sm, sinus maxillaris; sn, septum nasi;
st, septoturbinal. Scale bars equal 2 mm.
In the adult Tupaia several differences become evident. The lamina
semicircularis is rostrally bifurcated, and thus the anterior tip of the
recessus frontoturbinalis is separated from the maxillary sinus (Figs. 4c, d,
7f) (see below). The lamina shows a sharp central bent into the paranasal
space (Fig. 8b). Tupaia also has a lateral and dorsally oriented
epiturbinal-like outgrowth, but it is separated from the lamina semicircularis
by a long fissure; posteriorly it fuses to the dorsal flank above the hiatus
semilunaris where it forms the hollow inflation of the dorsal flank's rim and
continues into a scroll (Figs. 8b, d, 9b, 10b). The processus uncinatus is
obviously much shorter in the fetal stages of Tupaia (Spatz, 1964;
Zeller, 1983, 1987) compared to Ptilocercus, but in the adults it
appears to be comparably developed (Figs. 4, 8d).
µCT cross-section images of the pars lateralis and
posterior of the adult rostrum from anterior to posterior of
(a) Ptilocercus lowii (ZMB 3992) and
(b) Tupaia sp. (collection W. Maier). Numbers in figures refer
to number of original µCT slices. Abbreviations: cla, canaliculus
lacrimalis; et I, II, ethmoturbinal I, II; ft 1, 2, frontoturbinal 1, 2; it,
interturbinal; ls, lamina semicircularis; M1, 2, upper molar 1, 2; mt,
maxilloturbinal; or, orbit; P3, upper premolar 3; po, pars obtecta (paries
conchalis); sm, sinus maxillaris; sn, septum nasi; st, septoturbinal. Scale
bars equal 2 mm.
Pars lateralis of nasal cavity
In the chondrocranium the pars lateralis (pars intermedia) of the ethmoidal
region is subdivided into two compartments by the lamina horizontalis (pars
obtecta of paries conchalis); the latter gives rise to most of the olfactory
turbinals (Voit, 1909; Reinbach, 1952a, b). The primary sidewall of the pars
lateralis but also of the pars posterior is called the pars libera. The
dorsal compartment is the recessus lateralis superior, which includes the
posterior recessus frontoturbinalis that houses the frontoturbinals and the
anterior recessus frontalis. Rostrally it is confluent with the ventral
space, the so-called recessus lateralis inferior (recessus maxillaris). This
space is the precursor of the sinus maxillaris in the adult; it houses two
large nasal glands: the serous glandula nasi lateralis and the mucous
glandula sinus maxillaris (Broman, 1921; Ruf, 2004). Medially the pars
lateralis is limited by the lamina semicircularis and the first
ethmoturbinal. Both recessus are confluent with the paraseptal space via the
hiatus semilunaris. The Scandentia under study resemble this general therian
pattern (Figs. 2, 4a–d).
The lamina horizontalis of the Ptilocercus fetus is rostrally
prolonged by a septum frontomaxillare. Comparing the fetal stages of
Ptilocercus and Tupaia belangeri it is evident that the
former has a smaller recessus lateralis superior than the latter. In the
adult Ptilocercus the pars obtecta shows several specific small
ventral ridges (Fig. 9a).
µCT cross-section images of the pars lateralis and
posterior of the adult rostrum from anterior to posterior of
(a) Ptilocercus lowii (ZMB 3992) and
(b) Tupaia sp. (collection W. Maier). Numbers in figures refer
to number of original µCT slices. Abbreviations: cla, canaliculus
lacrimalis; dnp, ductus nasopharyngeus; et I, II, III, ethmoturbinal I, II,
III; fla, foramen lacrimale; ft 1, 2, frontoturbinal 1, 2; it, interturbinal;
lc, lamina cribrosa; ls, lamina semicircularis; M1, 2, upper molar 1, 2; or,
orbit; po, pars obtecta (paries conchalis); sm, sinus maxillaris; sn, septum
nasi; st, septoturbinal. Scale bars equal 2 mm.
Ptilocercus has two frontoturbinals which are already present in the
fetal stage (Figs. 2a, 6a). Frontoturbinal 1 is a distinct lamella that
starts on the anterior projection of the lamina horizontalis and curves
caudodorsally along the paries nasi to the roof of the nasal cavity. It fuses
to the lamina cribrosa at its posterior end. The second frontoturbinal is
shorter and less developed in the fetus. Frontoturbinal 2 is a low ridge that
starts more posteriorly on the paries nasi and runs more or less parallel but
below frontoturbinal 1. In the adult Ptilocercus both
frontoturbinals have significantly evolved and their rostral attachments have
changed (Fig. 4a, b). Frontoturbinal 1 has two anterior processus: a longer
medial one that starts anterior of the hiatus semilunaris between lamina
semicircularis and ethmoturbinal I and a shorter lateral one that projects
laterally of the lamina semicircularis into the confluent space of the
recessus frontalis and recessus maxillaris (Figs. 4b, 8a, b). Both processus
unite in the hiatus semilunaris and become the double scroll that is attached
to the lamina horizontalis for a very short way. Frontoturbinal 2 starts with
an anterior process that is inserted into the ventral scroll of
frontoturbinal 1 (Fig. 8b). It lies ventrally of the latter and attaches to
the lamina horizontalis forming the typical double scroll. Both
frontoturbinals are large double-scrolled structures, mushroom-like in cross
section, except for their anterior portions and are posteriorly fused to the
lamina cribrosa (Figs. 9a, 10a, 11a, 12a).
The adult Tupaia also has two frontoturbinals that generally
resemble the same pattern as in Ptilocercus (Figs. 4c, d, 8b, d, 9b,
10b, 11b, 12b). However, their shape differs significantly. Frontoturbinal 1
of Tupaia has only one anterior process lateral to the lamina
semicircularis; by attaching to the lamina horizontalis it becomes also a
double scroll, but the two laminae are much more coiled and therefore
obviously proportionally larger than in Ptilocercus (Figs. 4d, 8b,
d, 9b, 10b). Frontoturbinal 2 also starts with an anterior process that is
embraced by the ventral and a short third lamella of frontoturbinal 1
(Fig. 8d). Posteriorly this third lamella becomes the actual ventral scroll
whereas the former ventral lamella becomes reduced. Frontoturbinal 2 of
Tupaia is a single scroll that is curled medially (Figs. 8b, 9b,
10b, 11b, 12b).
The recessus lateralis inferior of Ptilocercus is a flat ovoid space
that is connected to the paraseptal medially. The sinus maxillaris of the
adult stage has expanded significantly. It starts together with the recessus
lateralis superior above the second upper molar. The posterior end of the
sinus continuous into the paraseptal space and the ductus nasopharyngeus.
Thus it is not distinct in the cleaned skull because no glands are present
that can be used as landmarks. The sinus maxillaris is still ovoid in shape
but changed to a more vertical orientation (Figs. 8a, c, 9a, 10a, 11a, 12a).
In the adult Tupaia the sinus maxillaris is a large cavity whose
anterior tip is separated from the recessus frontalis by a short bony plate
that is most probably an ossified septum frontomaxillare (Fig. 7f). The sinus
starts on the level of the first upper premolar and ends – contrary to the
pattern in Ptilocercus – as a closed space above the second upper
molar ventromedial of the orbit. Medially the sinus maxillaris is partly
confluent with the paraseptal space and the ductus nasopharyngeus. The sinus
is mostly rectangular in shape (Figs. 8b, d, 9b, 10b, 11b).
Further expansions of the nasal cavity into surrounding bones are not present
in any of the investigated Scandentia species, which possess neither frontal
sinus nor a distinct sphenoid sinus (as already observed by Negus, 1958, and
Wible, 2011). However, in the adult stage of Tupaia the spaces
between the lamina semicircularis, the frontoturbinals, and the brain cavity
itself bulge out distinctly as clearly seen in cross section (Figs. 8d, 9b,
10b). Thus based on external anatomy the existence of extensive frontal sinus
is indicated, which is apparently not the case. Perinatal ontogenetic stages
of Tupaia do not clearly show this feature yet.
Pars posterior of nasal cavity
The pars posterior comprises the recessus ethmoturbinalis that houses the
majority of the olfactory turbinals. Ptilocercus and Tupaia
both have three ethmoturbinals and one interturbinal (Figs. 2, 4). Though
more or less identical in rostrocaudal extension the pars posterior is
significantly wider in the Ptilocercus fetus than in the neonate of
Tupaia glis. The posterior portion of the nasal capsule of the fetal
Ptilocercus reaches the radix anterior of the pila praeoptica
(Fig. 1a). Thus a foramen supraseptale is separated from the fissura
orbitonasalis. In contrast the fetal stage of Tupaia does not show
any fragmentation of the fissura.
In the fetal Ptilocercus ethmoturbinal I is by far the largest
olfactory turbinal and already has two anterior portions: pars anterior and
pars posterior (Figs. 2a, 5b, 6a). The pars anterior projects into the pars
anterior of the nasal cavity with a processus anterior that is triangular in
cross section and pointed. In comparison the processus anterior of
Ptilocercus is proportionally longer than that of Tupaia glis (Fig. 2). The pars anterior of ethmoturbinal I is separated from the
pars posterior by a deep medial cavity (Fig. 6a). Both parts of the first
ethmoturbinal are simple lamellae in the fetal stage. The ethmoturbinal I is
connected to the pars obtecta of the paries conchalis and ends on the lamina
cribrosa (Fig. 6b).
In the adult Ptilocercus the first ethmoturbinal has become a
complex structure. Both parts of ethmoturbinal I are extremely different in
size. More than half of the turbinal is represented by the processus anterior
of the pars anterior and the pars posterior is extremely short (Fig. 4a). The
processus anterior projects far into the pars anterior of the nasal cavity.
In contrast to the fetus the process is a lamella from the beginning and
becomes a dome-shaped structure above the nasoturbinal and maxilloturbinal
(Fig. 7a, c, e). Further posteriorly the processus anterior completely
embraces the dorsal lamella of the maxilloturbinal (Figs. 7e, 8a). On a level
with the anterior rim of the hiatus semilunaris the dorsal part of the
processus anterior develops a sinus. The ventral portion is continuous with
the lamina horizontalis whereas the dorsal sinus of the processus anterior
becomes the medially curled lamella of the pars anterior. The pars posterior
starts with an anterior process between septum nasi and pars anterior of
ethmoturbinal I (Fig. 8c). Anteriorly it forms a vertical sinus that develops
a ventral lamella. The latter becomes incorporated into the lamina
horizontalis. The dorsal hollow portion of the pars posterior transforms into
a laterally curled lamella that is nested in the scroll of the pars anterior
(Fig. 9a). Anteriorly the pars posterior is fused to the lamina horizontalis
but then originates from the proximal pars anterior (Figs. 9a, 10a, 11a,
12a).
Ethmoturbinal I of Tupaia shows some different proportions. As
already observed in fetal stages the pars posterior is proportionally larger
than in Ptilocercus (Figs. 4c, 7b, d, f, 8b, d, 9b, 10b, 11b, 12b).
µCT cross-section images of the pars lateralis and
posterior of the adult rostrum from anterior to posterior of
(a) Ptilocercus lowii (ZMB 3992) and
(b) Tupaia sp. (collection W. Maier). Numbers in figures refer
to number of original µCT slices. Abbreviations: dnp, ductus
nasopharyngeus; et I, II, III, ethmoturbinal I, II, III; ft 1, 2,
frontoturbinal 1, 2; it, interturbinal; lc, lamina cribrosa; M1, 2, upper
molar 1, 2; or, orbit; sm, sinus maxillaris; sn, septum nasi; st,
septoturbinal; vo, vomer. Scale bars equal 2 mm.
The ethmoturbinal II is a sagittal lamella in the fetus of
Ptilocercus (Fig. 2a). Rostrally it originates from the pars obtecta
but runs caudolaterally onto the pars libera. Its posterior end fuses to the
lamina cribrosa. Laterally the ethmoturbinal II shows a second lamella.
In the adult stage of Ptilocercus the second ethmoturbinal has an
anterior process that projects anteriorly between interturbinal and septum
nasi. The tip of the processus anterior is a vertical lamella that increases
posteriorly and develops a dorsal cavity (Figs. 4a, 9a). This cavity opens
laterally; thus the anterior process of ethmoturbinal II becomes L-shaped.
Further posterior the dorsal part of the process curls laterally and fuses
to a second processus anterior. This second process is situated laterally
from the first one and its anterior tip projects into the hollowed base of
the interturbinal (Fig. 10a). The lateral anterior process is a horizontal
lamella that develops a medial short cavity that opens ventrally just in
front of the fusion of both processus. The ethmoturbinal II becomes a
complicated and multi-branched lamella (Figs. 11a, 12a). It appears to fuse
with the posterior end of the lamina horizontalis. However, there is a vague
transition from the lamina horizontalis to the base of ethmoturbinal III from
which ethmoturbinal II thus emerges before it runs on the sidewall of the
nasal cavity. From here on ethmoturbinal II is an oblique lamella that
connects to the lamina cribrosa and that has a lateral double scroll, further
posterior a single-scroll portion (Fig. 13a). Ethmoturbinal II of
Tupaia resembles the pattern observed in Ptilocercus though
it is proportionally larger in the former (Figs. 2b, 4c, 8d, 9b, 10b, 11b,
12b, 13b).
In the Ptilocercus fetus the ethmoturbinal III is a sickle-shaped
simple lamella that originates from the pars libera of the paries conchalis.
Caudally it is continuous with the lamina cribrosa (Fig. 2). In the adult
Ptilocercus the third ethmoturbinal has a triangular hollow
processus anterior that projects ventrally of the second ethmoturbinal
(Figs. 4c, 11a). Running posteriorly the cavity opens laterally and in
contrast to the fetal pattern the ventral part fuses to the presumably
posterior end of the lamina horizontalis and the base of ethmoturbinal II,
respectively, and thus forms a large horizontal plate that forms a scroll
dorsally. More posteriorly the base of ethmoturbinal III moves to the side
wall of the nasal cavity (Figs. 12a, 13a, 14a). Here the scroll of
ethmoturbinal III becomes complicated and the posterior part of the turbinal
is tripartite forming a mushroom-shaped double scroll in dorsal view. After
fusion to the lamina cribrosa the lateral part of the scroll becomes isolated
as a posterior process. Right before it ends the same happens to the medial
part of ethmoturbinal III (Fig. 14a). Thus the remaining ethmoturbinal forms
a septum that encloses a quadrangular cavity. The medial posterior process
ends with a cavity in the cupula nasi posterior (Fig. 15a).
µCT cross-section images of the pars posterior of the adult
rostrum from anterior to posterior of (a) Ptilocercus lowii
(ZMB 3992) and (b) Tupaia sp. (collection W. Maier). Numbers in
figures refer to number of original µCT slices. Abbreviations: dnp,
ductus nasopharyngeus; et I, II, III, ethmoturbinal I, II, III; ft 1, 2,
frontoturbinal 1, 2; it, interturbinal; lc, lamina cribrosa; M2, 3, upper
molar 2, 3; or, orbit; sm, sinus maxillaris; sn, septum nasi; st,
septoturbinal; vo, vomer. Scale bars equal 2 mm.
µCT cross-section images of the pars posterior of the adult
rostrum from anterior to posterior of (a) Ptilocercus lowii
(ZMB 3992) and (b) Tupaia sp. (collection W. Maier). Numbers in
figures refer to number of original µCT slices. Abbreviations: dnp,
ductus nasopharyngeus; et II, III, ethmoturbinal II, III; lc, lamina
cribrosa; lt, lamina terminalis; M2, 3, upper molar 2, 3; or, orbit; sn,
septum nasi. Scale bars equal 2 mm.
In general the third ethmoturbinal of Tupaia shows the same
morphology though some differences occur in the adult (Figs. 2b, 4c, 10b,
11b, 12b, 13b, 14b, 15b). Those affect the proportions and the anterior
process of ethmoturbinal III projecting into a proximal cavity of
ethmoturbinal II.
Between the first and second ethmoturbinal the fetus of Ptilocercus
already shows an interturbinal (Fig. 2a). It forms a distinct sagittal
cartilaginous ridge that runs from the pars obtecta to the lamina cribrosa.
Medially the interturbinal does not reach the same extension as the
ethmoturbinals, a pattern that defines interturbinals (see Paulli, 1900a).
In the adult Ptilocercus the interturbinal starts with an anterior
process that projects into a basal cavity at the base of the first turbinal.
The processus anterior itself forms more or less triangular cavity that opens
ventrally above the lamina horizontalis. In cross section the interturbinal
is a horizontal lamella that is curved dorsally in the middle. The
interturbinal fuses to a hollowed outgrowth of the lamina horizontalis that
represents the base or root of the interturbinal. However, only the lateral
portion becomes the interturbinal main body whereas the medial part is again
integrated into the lamina horizontalis (Fig. 10a). The interturbinal is a
simple scroll that is curled dorsally (Figs. 11a, 12a).
µCT cross-section images of the pars posterior of the adult
rostrum and orbit from anterior to posterior of
(a) Ptilocercus lowii (ZMB 3992) and
(b) Tupaia sp. (collection W. Maier). Numbers in figures refer
to number of original µCT slices. Abbreviations: dnp, ductus
nasopharyngeus; et III, ethmoturbinal III; lc, lamina cribrosa; lic, lamina
infracribrosa; lt, lamina terminalis; M2, upper molar 2; or, orbit; sn,
septum nasi. Scale bars equal 2 mm.
The interturbinal of the adult Tupaia is comparable to
Ptilocercus except for its anterior portion. Between the processus
anterior and the single scroll for a short distance, the interturbinal of
Tupaia is a double scroll, i.e. mushroom-shaped in cross section
(Figs. 8d, 9b, 10b, 11b, 12b).
The cupula nasi posterior forms the posterior end of the nasal cavity
(Figs. 1a, 2a). In the fetus of Ptilocercus it is still completely
cartilaginous and its radius is significantly larger than in the neonate
Tupaia (Zeller, 1983, 1987).
In the adult stage the cupula nasi posterior is completely ossified and
integrated in the surrounding bones of the orbit. In Ptilocercus the
cupula nasi posterior is rectangular in cross section whereas in
Tupaia it is laterally compressed (Fig. 15a, b).
µCT cross-section images of the cupula nasi posterior of
the adult rostrum and the anterior orbitotemporal region from anterior to
posterior of (a, c) Ptilocercus lowii (ZMB 3992)
and (b, d) Tupaia sp. (collection W. Maier). Numbers in
figures refer to number of original µCT slices. Abbreviations: bc,
basicranium; cnp, cupula nasi posterior; dnp, ductus nasopharyngeus; et III,
ethmoturbinal III; lic, lamina infracribrosa; lt, lamina terminalis; M3,
upper molar 3; or, orbit; sio, septum interorbitale. Scale bars equal 2 mm.
Solum nasi
The solum nasi (nasal floor) consists of several elements in the
chondrocranium: lamina transversalis anterior, cartilago paraseptalis (houses
the vomeronasal organ), and lamina transversalis posterior (Fig. 2). Here we
only refer to the lamina transversalis posterior, because the lamina
transversalis anterior is still cartilaginous in the adult and therefore not
visible in the µCT scan, and the cartilago paraseptalis is generally
replaced by the medial palatine process of the premaxilla and maxilla (see
Ruf, 2004).
The lamina transversalis posterior is a horizontal cartilaginous plate in the
fetal stage of Ptilocercus and separates the posterior end of the
nasal cavity from the ductus nasopharyngeus. From the septum nasi the entire
lamina transversalis posterior is separated by a distinct fissure. The vomer
lies beneath the septum nasi and the lamina transversalis posterior and fuses
partly with the latter. Laterally the lamina is continuous with the paries
nasi, posteriorly with the cupula nasi posterior.
In adult stages the lamina transversalis posterior is synossified with the
vomer. As both elements are not distinguishable the entire structure is
called lamina terminalis. In Ptilocercus the lamina terminalis is
V-shaped. Anteriorly it is continuous with the vomer and its alae. The
posterior half of the lamina terminalis bulges out into the ethmoturbinal
recess (Figs. 13a, 14a, 15a). In contrast the lamina terminalis of the adult
Tupaia is positioned horizontally (Figs. 11b, 12b, 13b, 14b, 15b).
Discussion
Ptilocercidae and Tupaiidae show many similar but also significantly
different cranial features which are associated with size and proportion of
the ethmoidal region and orbit orientation, and therefore correlated to the
behavioural biology of the investigated species.
Beside vision, olfaction is a major sense in nocturnal and arboreal mammals
especially for social and sexual communication (Epple et al., 1993).
Ptilocercus is an arboreal and nocturnal hunter; thus stereoscopic
vision is highly important while foraging on insects, which explains the
larger, more anteriorly positioned and frontally oriented orbits compared to
Tupaia. In contrast Tupaia species are mainly diurnal, most
of which forage on the ground and in bushes and thus stereoscopic vision
might be less important (Hofer, 1957; Cartmill, 1972; Sargis, 2001). Though
Scandentia have relatively large eyes the posterior ethmoidal region is not
reduced (see Smith et al., 2014b). Our new findings on the investigated
Scandentia support earlier observations on Tupaia that the nasal
cavity of Scandentia is well-developed and clearly indicates macrosmatic
sense, the ability of high
olfactory performance (Spatz, 1964; Zeller, 1987; Smith et al., 2014b).
Macrosmatic ability is a plesiomorphic mammalian character (see Maier and
Ruf, 2014), and many of the here described characters and ontogenetic
transformations are correlated with this feature and represent plesiomorphic
states for the clade Scandentia (Zeller, 1986b, 1987; Maier and Ruf, 2014;
Ruf, 2004, 2014).
Throughout ontogeny the ethmoidal region is proportionally longer in
Ptilocercus than in Tupaia, though a general expansion
occurs in postnatal growth of both taxa. The crucial differences in
proportion of the posterior ethmoidal region of the investigated Scandentia,
such as shape of lamina cribrosa, shape of lamina horizontalis, crista galli and
spina mesethmoidalis in Tupaia, are caused by size and orientation
of the orbits and interaction with associated structures of the olfactory
nervous system. The nasal capsule of Ptilocercus is relatively
longer than in Tupaia and shows different proportions. The pars
posterior of the Ptilocercus fetal nasal cavity is slightly longer
than the pars anterior whereas in Tupaia both compartments are
similar in length. Much more evident are proportional differences concerning
the width of the nasal cavities. Ptilocercus has a wider pars
posterior than Tupaia. The lamina cribrosa shows a complementary
pattern: the area that leads the fila olfactoria of the ethmoidal recess is
wider in Ptilocercus than in Tupaia, thus indicating a
greater olfactory importance of the ethmoturbinals in Ptilocercus.
A macrosmatic ethmoidal region is reduced or even lost in certain mammalian
clades, e.g. in cetaceans (Klima, 1999; Berta et al., 2014). Primates,
another striking example, show the evolutionary tendency to highly reduce
number and complexity of turbinals due to adaptations to an arboreal life
along with stereoscopic vision. Thus, not only is olfaction less important in
haplorhine primates but also the enlarged eyes and rostrally oriented orbits
are conflicting with the posterior nasal capsule in terms of the demand for
space (Maier, 1983; Maier and Ruf, 2014). However, Scandentia have an
elaborated ethmoidal region with well-developed olfactory turbinals which is
obviously not in spatial conflict with the enlarged eyes (Smith et al.,
2014b). As skull size, chewing apparatus, basicranial kyphosis, and
proportion of the brain cavity are comparable in Ptilocercus and
Tupaia, these factors obviously do not influence the morphology of
the anterior basicranium, i.e. the existence of a septum interorbitale in the
latter (Haines, 1950; Spatz, 1964, 1970; Starck, 1979; see discussion below).
Thus, the most striking features to be discussed are the internal
organization of the nasal in terms of turbinals as well as the pattern of the
posterior tip of the ethmoidal region, the occurrence of a
septum interorbitale.
Turbinal pattern
The nasal capsule of mammals shows a quite uniform Bauplan in early
ontogeny though it becomes modified with often highly complex ossified
structures and partly resorbed in later stages (Maier and Ruf, 2014). In
general the ethmoidal region of Ptilocercus resembles the pattern
observed in Tupaia. Comparing the proportions of the ossified
turbinals in the adult skull of Ptilocercus and Tupaia it
is evident that in the former the fronto- and ethmoturbinals as well as the
interturbinal are proportionally smaller (shorter) than in the latter. The
demand for space of the orbits in Ptilocercus restricts the lateral
parts of the nasal cavity that results in a narrower ethmoidal region that
elongates posteriorly as far as the anterior border of the pila praeoptica in
the fetus. Furthermore, the frontoturbinals of Ptilocercus are less
developed than in Tupaia due to the fact that the pars lateralis and
therefore the frontoturbinal recess are larger in the latter. This shift in
proportions leads to the incorporation of the skull base between cupula nasi
posterior and pila praeoptica in the nasal capsule, whereas in
Tupaia the equivalent structure forms the septum interorbitale.
Thus, the observed differences in the proportions of the pars posterior might
serve as compensation.
The observed number of olfactory turbinals (two frontoturbinals, three
ethmoturbinals, one interturbinal between ethmoturbinal I and II) in
Ptilocercus does not support the data provided by Le Gros
Clark (1926) and Wible (2011). While the former describes two ectoturbinals
in the pars lateralis that correspond to the two frontoturbinals,
Wible (2011) reports three ectoturbinals. We can clearly demonstrate that
this interpretation is not correct. Wible's three lateral ectoturbinals
obviously comprise the lamina semicircularis and the two frontoturbinals.
Both authors describe four ethmoturbinals in the pars posterior. Our
investigation clearly demonstrates that Ptilocercus has only three
ethmoturbinals. Obviously the interturbinal has been erroneously included
into the ethmoturbinals by Le Gros Clark (1926) and Wible (2011). These
results clearly demonstrate the advantage of µCT-based
investigations of adult nasal cavities to enhance the three-dimensional
understanding of bony structures. Furthermore as already mentioned above the
consistent use of an adequate terminology is demanded in nasal anatomy.
All investigated species of Tupaia have the same number of turbinals
as Ptilocercus. Thus we can confidently conclude that two
frontoturbinals, and three ethmoturbinals plus one interturbinal represent
the morphotype of Scandentia. This pattern is also observed in many
small-sized mammals but especially in members of the Euarchontoglires like
many leporids, rodents, and Dermoptera (Paulli, 1900c; Voit, 1909; Frick and
Heckmann, 1955; Zeller, 1987; Ruf, 2004, 2014; Maier and Ruf, 2014).
Therefore the ethmoidal pattern of Scandentia may represent the plesiomorphic
ground plan pattern (sensu Hennig, 1950) of Euarchontoglires and at least a
more general pattern of placental mammals. However, body size also influences
the available space in the nasal cavity and therefore may constrain the
turbinal pattern. The absence of frontal sinuses in Scandentia would support
this idea as this type of sinus is also absent or rudimentarily developed in
many other small mammals (Paulli, 1900b, c; see Curtis and Van Valkenburgh,
2014a, for more details). Major differences in the turbinal pattern of the
investigated Scandentia are related to the size and topography of the
nasoturbinal, size and shape of frontoturbinal 2 and interturbinal (single
or double scroll) and the formation of anterior processus of certain
turbinals. The septoturbinal might be a synapomorphic feature though it shows
a different ontogenetic pattern in Ptilocercus and Tupaia.
Schematic horizontal section of the fetal nasal capsule and
basicranium of the orbitotemporal region of Tupaia (left) and
Ptilocercus (right) to illustrate the arrangement of the
septum interorbitale and adjacent structures that are influenced by
orientation of the eye ball and orbit. Abbreviations: ao, ala orbitalis; ca,
cartilago antorbitalis; eb, eye ball; fo, foramen opticum; nc, nasal capsule;
pa, pars anterior; pim, pila metoptica; pip, pila praeoptica; pl, pars
lateralis; pp, pars posterior; rapip, radix anterior pilae
praeopticae; sio, septum interorbitale; sn, septum nasi; tp, trabecular plate.
Nevertheless, the ethmoidal region of Scandentia helps to elucidate the
primate morphotype. The enigmatic aye-aye Daubentonia madagascariensis represents a basal clade of the Madagascan Strepsirhini,
but its olfactory turbinal skeleton is by far the most complicated among
primates (Maier, 1993b; Perelman et al., 2011; Roos et al., 2004; Maier and
Ruf, 2014). It has three frontoturbinals and four interturbinals in the
frontoturbinal recess as well as three ethmoturbinals and two interturbinals
in the ethmoidal recess. However, all other primates have less complex nasal
cavities, especially Platyrrhini (see Maier and Ruf, 2014). Thus the
Daubentonia nasal pattern could be a highly derived character state
as adaptation to its specialized foraging mode or it may represent a
plesiomorphic pattern inherited from the ancestor of Euarchontoglires (Maier
and Ruf, 2014). The latter hypothesis is supported by the fact that many
basal placental mammals like Xenarthra and members of the clade Afrotheria
have a significantly higher number of olfactory turbinals ranging from 4–5
frontoturbinals and 4–8 ethmoturbinals in xenarthrans (Paulli, 1900c;
Reinbach, 1952a, b; Schneider, 1955) and 4–9 frontoturbinals and 4–13
ethmoturbinals in afrotherians (Paulli, 1900b; Stoessel et al., 2010). The
number of interturbinals between fronto- and ethmoturbinals is extremely
increased, especially in Proboscidea. Interestingly small- to medium-sized
afrotherians show a lower number of olfactory turbinals, which resembles more
or less the pattern observed in the presumed
euarchontogliran morphotype.
In Hyracoidea three frontoturbinals and three ethmoturbinals are present
(Paulli, 1900c; Stoessel et al., 2010). Investigated members of the
Afrosoricida have two frontoturbinals and three ethmoturbinals (Paulli,
1900c; Roux, 1947). Though most molecular phylogenies place Afrosoricida not
at the base of the afrotherian clade (Murphy et al., 2001; Springer et al.,
2003; Bininda-Emonds et al., 2007; Meredith et al., 2011), their number of
turbinals could reflect a general placental pattern. Our new observations on
Ptilocercus confirm the turbinal morphotype already presumed for
Scandentia and in addition the hypothesis already preferred by Maier and
Ruf (2014) – i.e. Daubentonia secondarily increased its number of
turbinals.
Septum interorbitale
A septum interorbitale is generally present in “reptiles” and non-mammalian
synapsids (Weber, 1927; Romer, 1956). Thus, these taxa have a tropibasic
skull, i.e. a broad anterior skull base and widely separated orbits.
According to Gaupp (1900) the formation of the septum interorbitale in
reptiles and the mammalian ancestors is limited among other factors by the
size and topography of the orbits as well as the small olfactory organ.
During mammalian evolution the septum interorbitale becomes incorporated into
the cupula nasi posterior due to the caudally expanding nasal cavity in
addition to the intensive development of the telencephalon. Thus the
septum interorbitale becomes part of the septum nasi and the cupula nasi posterior.
The primarily tropibasic basicranium of microsmatic reptiles and basal
synapsids becomes secondarily platybasic in macrosmatic mammals (Gaupp, 1900;
Starck, 1979).
Concerning Euarchontoglires the distribution of a septum interorbitale across
the major clades is puzzling. In Ptilocercidae the rostral portion of the
primary basicranium forms a trabecular plate (Trabekelplatte) and
therefore it is platybasic. Tupaiidae have a septum interorbitale and a
tropibasic cranium. A comparative topography of the fetal nasal capsule and
anterior basicranium of Ptilocercus and Tupaia is presented
in Fig. 16. Several authors interpret the septum interorbitale of
Tupaia as a primate character (Saban, 1957; Spatz, 1964; Starck,
1975) and thus a synapomorphy of Scandentia and Primates, because they were
not aware of the pattern in Ptilocercus. Henckel (1928) did not
observe a septum interorbitale in a 20 mm CRL fetus of Tupaia javanica. Hence, he separated Scandentia from Primates. However, this result
was disproved by Zeller (1983), who described a distinct septum in the
respective specimen. Many investigations have revealed that the
septum interorbitale of primates shows a certain level of plasticity as a
non-uniform morphological structure and thus resembles an equivocal character
for systematic analyses of this order (Frets, 1914; Haines, 1950; Starck,
1953, 1960, 1975, 1979, 1984; Maier, 1983; Schneck, 1986). For instance, the
septum interorbitale can be present only in certain ontogenetic stages as
observed in Propithecus (Starck, 1962).
Absence of a septum interorbitale in Dermoptera is indicated by lack of this
structure in a fetal Galeopithecus temmincki (now
Galeopterus variegatus) (Henckel,
1929), but no data are available on adult stages. In contrast, many Rodentia
and all investigated Lagomorpha have a septum interorbitale (e.g. Voit, 1909;
Schrenk, 1989; Ruf, 2004, I. Ruf, personal observation, 2015); therefore a
septum interorbitale might be a ground plan character of Glires.
Polarization of the septum interorbitale in terms of apomorphic versus
plesiomorphic ground plan character states of euarchontogliran major clades
depends on which phylogeny is applied and still remains ambiguous.
Furthermore, the ontogenetic transformation of the anterior floor of the
braincase has to be taken into account. In many moderate macrosmatic mammals
(e.g. lemurs, Chiroptera, certain Eulipotyphla) the incorporation of the
septum interorbitale in the nasal capsule is not complete and therefore a
short septum interorbitale is still present, which resembles a primary
septum interorbitale (plesiomorphy). In contrast mammals like higher primates,
which have an evolved vision as a dominating sense and hence a reduced
olfactory organ, show a reduction of the nasal capsule and therefore a
recurrence of a septum interorbitale, which represents a secondary structure
(apomorphy). The latter was already incorporated in the nasal capsule in
their ancestors (Starck, 1979; Maier, 1983, 1986). Thus, not in all taxa does
the septum interorbitale represent a primitive (plesiomorphic) mammalian
feature.
In general frontal orientation of the orbits is assumed to be correlated with
an arboreal lifestyle because the resulting stereoscopic vision supports fast
climbing and jumping in a complex three-dimensional environment like a tree
(Collins, 1921; Howells, 1947). However, many small non-primate mammals exist
that do not show such adaptations, e.g. tree squirrels (Cartmill, 1970,
1972). Therefore, Cartmill (1972) proposes that the orbital orientation in
primates and tree shrews is exclusively constrained by stereoscopic vision
used for optical control during foraging. There are conflicting hypotheses
about the correlation of the orbit size and the existence of the
septum interorbitale. According to Starck (1979) orbit size influences the
development of a septum interorbitale whereas Spatz (1970) concludes that the
frontal orientation of the orbit is the major constraint. However, in
Ptilocercus the relatively large orbit and its frontal orientation
results in the opposite pattern: a trabecular plate instead. Ontogenetic
studies have shown that the development of the septum interorbitale is
constrained by the adjustment and demand for space of adjacent structures.
For example in prosimians we observe a similar pattern: Loris has a
septum interorbitale whereas Indri is lacking this structure though
its orbits are larger and more frontally oriented than in the former (Starck,
1953). According to Starck (1953) the pattern of Indri is correlated
with the larger nasal cavity and telencephalon. The septum interorbitale of
Saimiri is significantly increased and becomes perforated during
postnatal ontogeny forming a fenestra interorbitalis (Maier, 1983).
The laterally oriented orbits of Tupaia resemble a
plesiomorphic pattern of placental
mammals and Scandentia. In contrast Ptilocercus is highly
specialized in being strictly arboreal and having therefore frontally
oriented eyes. Thus, against the background of the similarly sized nasal
cavities of the investigated Scandentia and the septum interorbitale pattern
among other Euarchontoglires, the proportion of the ethmoidal region and the
occurrence of a septum interorbitale in Tupaia, which are influenced
by the orientation of the orbits, represent plesiomorphic features of
Tupaiidae and Scandentia in general. Ptilocercus has lost the
septum interorbitale which is a derived and therefore autapomorphic character
state of Ptilocercidae. Furthermore, in early ontogeny Ptilocercus
shows a foramen supraseptale that also represents an autapomorphic character
of the respective family.
In conclusion the new data on the comparative anatomy and ontogeny of the
ethmoidal region in Scandentia reveals new insight into the understanding of
primate evolution. This refers especially to the septum interorbitale. As
already suggested by Zeller (1986b) the ethmoidal region of Scandentia can
hardly be used for elucidating systematic relationships to the order Primates
as to the many plesiomorphic characters of the former. However, our
interpretation of the ontogeny of the posterior nasal capsule and of the
occurrence of the septum interorbitale clearly shows that the
septum interorbitale is most probably not a synapomorphy of Scandentia and Primates
and therefore has evolved independently in both orders. For consideration of
the septum interorbitale as a systematic and/or phylogenetic relevant feature,
it is not sufficient to simply refer to the presence or absence of this
structure. Only further detailed ontogenetic and morphological studies across
all major clades of Euarchontoglires are necessary to clarify the primary or
secondary nature of the septum interorbitale in the respective taxa as well
as other transformations during ontogeny (e.g. loss of the septum).