Growth and microanatomy of the paranasal sinuses in two species of New World monkeys.

Paranasal sinuses of living apes and humans grow with positive allometry, suggesting a novel mechanism for bone enlargement. Here, we examine the paranasal sinuses of the owl monkey (Aotus spp.) and a tamarin (Saguinus midas) across postnatal development. The prediction that paranasal sinuses grow disproportionately faster than the main nasal chamber is tested. We used diffusible iodine-based contrast-enhanced computed tomography and histology to study sinuses in eight Aotus and three tamarins ranging from newborn to adult ages. Sinuses were segmented at the mucosa-air cavity interface and measured in volume. All sinuses were lined by a ciliated respiratory epithelium, except for the ethmoid air cells in Aotus, which are lined in part by olfactory epithelium. An age comparison indicates that only the maxillary sinus and ethmoid air cells are present in newborns, and two additional sinuses (invading the orbitosphenoid and the frontal bone), do not appear until late infancy or later. Comparing newborns and adults, the main nasal airway is 10 times larger in the adult Aotus and ~ 6.5 times larger in adult Saguinus. In contrast, the maxillary sinus far exceeds this magnitude of difference: 24 times larger in the adult Aotus and 46 times larger in adult Saguinus. The frontal sinuses add significantly to total paranasal space volume in both species, but this growth is likely delayed until juvenile age. Results suggest ethmoid air cells expand the least. These results support our prediction that most paranasal sinuses have a distinctly higher growth rate compared to the main nasal chamber.

Eptesicus nilssonii varangus subsp. nov. (Vespertilionidae, Chiroptera) from the Lower Pleistocene of the Taurida Cave in Crimea.

A new northern serotine bat Eptesicus nilssonii varangus subsp. nov. is described on the base of an incomplete skull and a mandibular fragment from the Lower Pleistocene deposits of the Taurida cave in the central Crimea. This is the earliest record of the species. The presence of E. nilssonii (Keyserling et Blasius, 1839) in the Early Pleistocene bat assemblage of the Taurida cave indicates that this species lived in the south of Eastern Europe before its spreading into Central and Southeastern Europe.

Rhinolophus mehelyi scythotauricus subsp. nov. (Rhinolophidae, Chiroptera) from the Lower Pleistocene of the Taurida Cave in Crimea.

A new extinct subspecies of the Mehely's horseshoe bat, Rhinolophus mehelyi scythotauricus subsp. nov., is described on the base of an incomplete skull from the Lower Pleistocene deposits of the Taurida cave in the central Crimea. It is the largest member of the R. euryale group. In terms of the evolutionary level, it is intermediate between Plio-Pleistocene R. mehelyi birzebbugensis Storch, 1974 and recent members of the species, but its large size and relatively narrow upper molars may indicate belonging to a separate phylogenetic lineage within R. mehelyi Matschie, 1901. R. mehelyi scythotauricus subsp. nov. is the first fossil record of the species in the Crimea; it is also one of the northernmost finds of R. mehelyi.

Early Pleistocene Horseshoe Bat Rhinolophus macrorhinus cimmerius subsp. nov. (Rhinolophidae, Chiroptera) from the Taurida Cave in Crimea.

Numerous remains (incomplete skull, cranial and mandibular fragments, and isolated teeth) of a large horseshoe bat of the Rhinolophus ferrumequinum group are described from the Lower Pleistocene depo-sits of the Taurida cave in the central Crimea. They are assigned to Rhinolophus macrorhinus cimmerius subsp. nov. In dental characters the new subspecies is less specialized than R. m. anomalidens Topál, 1979 from the Late Villafranchian of Central Europe, which implies the origin of the former from an earlier form morphologically close to R. m. macrorhinus Topál, 1963. The perfect preservation of the cranial structures made it possible to observe the remnants of the palatal ridges and the morphology of the nasal turbinals of R. macro-rhinus cimmerius subsp. nov.

Maxilloturbinal Aids in Nasophonation in Horseshoe Bats (Chiroptera: Rhinolophidae).

Horseshoe bats (Family Rhinolophidae) show an impressive array of morphological traits associated with use of high duty cycle echolocation calls that they emit via their nostrils (nasophonation). Delicate maxilloturbinal bones inside the nasal fossa of horseshoe bats have a unique elongated strand-like shape unknown in other mammals. Maxilloturbinal strands also vary considerably in length and cross-sectional shape. In other mammals, maxilloturbinals help direct respired air and prevent respiratory heat and water loss. We investigated whether strand-shaped maxilloturbinals in horseshoe bats perform a similar function to those of other mammals, or whether they were shaped for a role in nasophonation. Using histology, we studied the mucosa of the nasal fossa in Rhinolophus lepidus, which we compared with Hipposideros lankadiva (Hipposideridae) and Megaderma lyra (Megadermatidae). Using micro-CT scans of 30 horseshoe bat species, we quantified maxilloturbinal surface area and skull shape within a phylogenetic context. Histological results showed horseshoe bat maxilloturbinals are covered in a thin, poorly vascularized, sparsely ciliated mucosa poorly suited for preventing respiratory heat and water loss. Maxilloturbinal surface area was correlated with basicranial width, but exceptionally long and dorsoventrally flat maxilloturbinals did not show enhanced surface area for heat and moisture exchange. Skull shape variation appears to be driven by structures linked to nasophonation, including maxilloturbinals. Resting echolocation call frequency better predicted skull shape than did skull size, and was specifically correlated with dimensions of the rostral inflations, palate, and maxilloturbinals. These traits appear to form a morphological complex, indicating a nasophonatory role for the strand-shaped rhinolophid maxilloturbinals. Anat Rec, 2018. © 2018 American Association for Anatomy.

Anatomy of the olfactory system.

Of the principal sensory systems (vision, olfaction, taste, hearing, and balance), olfaction is one of the oldest. This ubiquitous system has both peripheral and central subdivisions. The peripheral subdivision is comprised of the olfactory epithelium and nerve fascicles, whereas the central subdivision is made up of the olfactory bulb and its central connections. Humans lack the "accessory olfactory system" of many other mammals, exhibiting only a nonfunctioning vestige of its peripheral element, the vomeronasal organ. Compared to most mammals, major elements of the human olfactory system are reduced; for example, humans have fewer turbinates than many mammals, and their olfactory epithelia are found only on one or two of these structures and their adjacent surfaces. Nonetheless, humans retain a full complement of functional cellular elements including a regenerating population of olfactory sensory neurons. These neurons extend long ciliary processes into the mucus that form a mat of cilia on which the odorant receptors are located. The olfactory sensory neurons send their axons directly to synapse within the olfactory bulb. Mitral and tufted cells then relay impulses from the bulb to other brain regions. This chapter describes the general anatomy and microanatomy of the olfactory system.

Unique Turbinal Morphology in Horseshoe Bats (Chiroptera: Rhinolophidae).

The mammalian nasal fossa contains a set of delicate and often structurally complex bones called turbinals. Turbinals and associated mucosae function in regulating respiratory heat and water loss, increasing surface area for olfactory tissue, and directing airflow within the nasal fossa. We used high-resolution micro-CT scanning to investigate a unique maxilloturbinal morphology in 37 species from the bat family Rhinolophidae, which we compared with those of families Hipposideridae, Megadermatidae, and Pteropodidae. Rhinolophids exhibit numerous structural modifications along the nasopharyngeal tract associated with emission of high duty cycle echolocation calls via the nostrils. In rhinolophids, we found that the maxilloturbinals and a portion of ethmoturbinal I form a pair of strand-like bony structures on each side of the nasal chamber. These structures project anteriorly from the transverse lamina and complete a hairpin turn to project posteriorly down the nasopharyngeal duct, and vary in length among species. The strand-like maxilloturbinals in Rhinolophidae were not observed in our outgroups and represent a synapomorphy for this family, and are unique in form among mammals. Within Rhinolophidae, maxilloturbinal size and cross-sectional shape were correlated with phylogeny. We hypothesize that strand-shaped maxilloturbinals may function to reduce respiratory heat and water loss without greatly impacting echolocation call transmission since they provide increased mucosal surface area for heat and moisture exchange but occupy minimal space. Alternatively, they may play a role in transmission of echolocation calls since they are located directly along the path sound travels between the larynx and nostrils during call emission. Anat Rec, 300:309-325, 2017. © 2016 Wiley Periodicals, Inc.

Tour of a labyrinth: exploring the vertebrate nose.

This special issue of The Anatomical Record is the outcome of a symposium entitled "Inside the Vertebrate Nose: Evolution, Structure and Function." The skeletal framework of the nasal cavity is a complicated structure that often houses sinuses and comprises an internal skeleton of bone or cartilage that can vary greatly in architecture among species. The nose serves multiple functions, including olfaction and respiratory air-conditioning, and its morphology is constrained by evolution, development, and conflicting demands on cranial space, such as enlarged orbits. The nasal cavity of vertebrates has received much more attention in the last decade due to the emergence of nondestructive methods that allow improved visualization of the internal anatomy of the skull, such as high-resolution x-ray computed tomography and magnetic resonance imaging. The 17 articles included here represent a broad range of investigators, from paleontologists to engineers, who approach the nose from different perspectives. Key topics include the evolution and development of the nose, its comparative anatomy and function, and airflow through the nasal cavity of individual species. In addition, this special issue includes review articles on anatomical reduction of the olfactory apparatus in both cetaceans and primates (the vomeronasal system), as well as the molecular biology of olfaction in vertebrates. Together these articles provide an expansive summary of our current understanding of vertebrate nasal anatomy and function. In this introduction, we provide background information and an overview of each of the three primary topics, and place each article within the context of previous research and the major challenges that lie ahead.

Morphology of the nasal capsule of primates--with special reference to Daubentonia and Homo.

Primitive mammals are considered macrosmatic. They have very large and complicated nasal capsules, nasal cavities with extensive olfactory epithelia, and relatively large olfactory bulbs. The complicated structures of the nasal capsule follow a relatively conservative "bauplan," which is normally easy to see in earlier fetal stages; especially in altricial taxa it differentiates well into postnatal life. As anteriormost part of the chondrocranium, the nasal capsule is at first cartilaginous. Most of it ossifies endochondrally, but "appositional bone" ("Zuwachsknochen") is also common. Many fetal structures become resorbed. Together, all surviving bone structures form the ethmoid bone, but cartilages of the external nose and of the vomeronasal complex can persist throughout life. We describe in detail the anatomy of Daubentonia madagascariensis based on a fetal stage (41 mm HL) and an adult skull was analyzed by µCT. We found that the nasal capsule of this species is by far the most complicated one of all extant Primates. We also describe older fetuses of Homo sapiens (35 and 63 mm HL) as representative of a derived primate. The most significant feature of man--and probably of all anthropoids--is the complete loss of the recessus frontoturbinalis and its associated structures. It can be demonstrated that the evolutionary reductions within the primate nasal capsule mainly affect those structures associated with olfaction, whereas cartilages that are important for the biomechanics of the facial skull of the fetus persist.

Nasal anatomy of the non-mammaliaform cynodont Brasilitherium riograndensis (Eucynodontia, Therapsida) reveals new insight into mammalian evolution.

The mammalian nasal cavity is characterized by a unique anatomy with complex internal features. The evolution of turbinals was correlated with endothermic and macrosmatic adaptations in therapsids and in early mammals, which is still apparent in their twofold function (warming and moistening of air, olfaction). Fossil evidence for the transformation from the nonmammalian to the mammalian nasal cavity pattern has been poor and inadequate. Ossification of the cartilaginous nasal capsule and turbinals seems to be a feature that occurred only very late in synapsid evolution but delicate ethmoidal bones are rarely preserved. Here we provide the first µCT investigation of the nasal cavity of the advanced non-mammaliaform cynodont Brasilitherium riograndensis from the Late Triassic of Southern Brazil, a member of the sister-group of mammaliaforms, in order to elucidate a critical anatomical transition in early mammalian evolution. Brasilitherium riograndensis already had at least partially ossified turbinals as remnants of the nasoturbinal and the first ethmoturbinal are preserved. The posterior nasal septum is partly ossified and contributes to a mesethmoid. The nasal cavity is posteriorly expanded and forms a distinctive pars posterior (ethmoidal recess) that is ventrally separated from the nasopharyngeal duct by a distinct lamina terminalis. Thus, our observations clearly demonstrate that principal features of the mammalian nasal cavity were already present in the sister-group of mammaliaforms.

Comparative anatomy and systematic implications of the turbinal skeleton in Lagomorpha (Mammalia).

In order to elucidate the systematic relevance of the turbinal skeleton in Lagomorpha the ethmoidal regions of 6 ochotonid, 21 leporid, and 2 outgroup species (Sciurus vulgaris, Tupaia sp.) species were investigated by high-resolution computed tomography (µCT). Number and shape of turbinals correspond to major clades and to several genera. All Lagomorpha under study have a deeply excavated nasoturbinal that is continuous with the lamina semicircularis; a feature likely to be an autapomorphy of lagomorphs. In particular, the olfactory turbinals (frontoturbinals, ethmoturbinals, and interturbinals) provide new systematic information. The plesiomorphic lagomorph pattern comprises two frontoturbinals, three ethmoturbinals, and one interturbinal between ethmoturbinal I and II. Ochotonidae are derived from the lagomorph goundplan by loss of ethmoturbinal III; an interturbinal between the two frontoturbinals is an autapomorphy of Leporidae. Pronolagus is apomorphic in having a very slender first ethmoturbinal, but shows a puzzling pattern in decreasing the number of turbinals. Pronolagus rupestris and Romerolagus diazi have independently reduced their turbinals to just two fronto- and two ethmoturbinals, which is the lowest number among the sampled lagomorphs. In contrast, the more derived leporid genera under study (Oryctolagus, Caprolagus, Sylvilagus, and Lepus) show a tendency to increase the number of turbinals, either by developing an ethmoturbinal IV (Caprolagus hispidus, Lepus arcticus) or by additional interturbinals. Intraspecific variation was investigated in Ochotona alpina, Oryctolagus cuniculus, and Lepus europaeus and is restricted to additional interturbinals in the frontoturbinal recess of the two leporids.

The shrinking anthropoid nose, the human vomeronasal organ, and the language of anatomical reduction.

Humans and most of our closest extant relatives, the anthropoids, are notable for their reduced "snout." The striking reduction in facial projection is only a superficial similarity. All anthropoids, including those with long faces (e.g., baboons), have lost numerous internal projections (turbinals) and spaces (recesses). In sum, this equates to the loss of certain regions of olfactory mucosa in anthropoids. In addition, an accessory olfactory organ, the vomeronasal organ, is non-functional or even absent in all catarrhine primates (humans, apes, monkeys). In this commentary, we revisit the concept of anatomical reductions as it pertains to the anthropoid nasal region. Certain nasal structures and spaces in anthropoids exhibit well-known attributes of other known vestiges, such as variability in form or number. The cupular recess (a vestige of the olfactory recess) and some rudimentary ethmoturbinals constitute reduced structures that presumably were fully functional in our ancestors. Humans and at least some apes retain a vestige that is bereft of chemosensory function (while in catarrhine monkeys it is completely absent). However, the function of the vomeronasal system also includes prenatal roles, which may be common to most or all mammals. Notably, neurons migrate to the brain along vomeronasal and terminal nerve axons during embryogenesis. The time-specific role of the VNO raises the possibility that our concept of functional reduction is too static. The vomeronasal system of humans and other catarrhine primates appears to qualify as a "chronological" vestige, one which fulfills part of its function during ontogeny, and then becomes lost or vestigial.