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Our knowledge of nasal cavity anatomy has grown considerably with the advent of micro-computed tomography (CT). More recently, a technique called diffusible iodine-based contrast-enhanced CT (diceCT) has rendered it possible to study nasal soft tissues. Using diceCT and histology, we aim to (a) explore the utility of these techniques for inferring the presence of venous sinuses that typify respiratory mucosa and (b) inquire whether distribution of vascular mucosa may relate to specialization for derived functions of the nasal cavity (i.e., nasal-emission of echolocation sounds) in bats. Matching histology and diceCT data indicate that diceCT can detect venous sinuses as either darkened, "empty" spaces, or radio-opaque islands when blood cells are present. Thus, we show that diceCT provides reliable information on vascular distribution in the mucosa of the nasal airways. Among the bats studied, a nonecholocating pteropodid (Cynopterus sphinx) and an oral-emitter of echolocation sounds (Eptesicus fuscus) possess venous sinus networks that drain into the sphenopalatine vein rostral to the nasopharynx. In contrast, nasopharyngeal passageways of nasal-emitting hipposiderids are notably packed with venous sinuses. The mucosae of the nasopharyngeal passageways are far less vascular in nasal-emitting phyllostomids, in which vascular mucosae are more widely distributed in the nasal cavity, and in some nectar-feeding species, a particularly large venous sinus is adjacent to the vomeronasal organ. Therefore, we do not find a common pattern of venous sinus distribution associated with nasal emission of sounds in phyllostomids and hipposiderids. Instead, vascular mucosa is more likely critical for air-conditioning and sometimes vomeronasal function in all bats., (© 2021 American Association for Anatomy.)

Living primates show a complex trend in reduction of nasal cavity spaces and structures due to moderate to severe constraint on interorbital breadth. Here we describe the ontogeny of the posterior end of the primate cartilaginous nasal capsule, the thimble shaped posterior nasal cupula (PNC), which surrounds the hind end of the olfactory region. We used a histologically sectioned sample of strepsirrhine primates and two non-primates (Tupaia belangeri, Rousettus leschenaulti), and histochemical and immunohistochemical methods to study the PNC in a perinatal sample. At birth, most strepsirrhines possess only fragments of PNC, and these lack a perichondrium. Fetal specimens of several species reveal a more complete PNC, but the cartilage exhibits uneven or weak reactivity to type II collagen antibodies. Moreover, there is relatively less matrix than in the septal cartilage, resulting in clustering of chondrocytes, some of which are in direct contact with adjacent connective tissues. In one primate (Varecia spp.) and both non-primates, the PNC has a perichondrium at birth. In older, infant Varecia and Rousettus, the perichondrium of the PNC is absent, and PNC fragmentation at its posterior pole has occurred in the former. Loss of the perichondrium for the PNC appears to precede resorption of the posterior end of the nasal capsule. These results suggest that the consolidation of the basicranial and facial skeletons happens ontogenetically earlier in primates than other mammals. We hypothesize that early loss of cartilage at the sphenoethmoidal articulation limits chondral mechanisms for nasal complexity, such as interstitial expansion or endochondral ossification., (© 2021 American Association for Anatomy.)

Mammalian nasal capsule development has been described in only a few cross-sectional age series, rendering it difficult to infer developmental mechanisms that influence adult morphology. Here we examined a sample of Leschenault's rousette fruit bats (Rousettus leschenaultii) ranging in age from embryonic to adult (n = 13). We examined serially sectioned coronal histological specimens and used micro-computed tomography scans to visualize morphology in two older specimens. We found that the development of the nasal capsule in Rousettus proceeds similarly to many previously described mammals, following a general theme in which the central (i.e., septal) region matures into capsular cartilage before peripheral regions, and rostral parts of the septum and paries nasi mature before caudal parts. The ossification of turbinals also generally follows a rostral to the caudal pattern. Our results suggest discrete mechanisms for increasing complexity of the nasal capsule, some of which are restricted to the late embryonic and early fetal timeframe, including fissuration and mesenchymal proliferation. During fetal and early postnatal ontogeny, appositional and interstitial chondral growth of cartilage modifies the capsular template. Postnatally, appositional bone growth and pneumatization render greater complexity to individual structures and spaces. Future studies that focus on the relative contribution of each mechanism during development may draw critical inferences how nasal morphology is reflective of, or deviates from the original fetal template. A comparison of other chiropterans to nasal development in Rousettus could reveal phylogenetic patterns (whether ancestral or derived) or the developmental basis for specializations relating to respiration, olfaction, or laryngeal echolocation., (© 2020 American Association for Anatomy.)

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., (© 2018 American Association for Anatomy.)

Living primates have relatively large eyes and support orbital tissues with a postorbital bar (POB) and/or septum. Some mammals with large eyes lack a POB, and presumably rely on soft tissues. Here, we examined the orbits of four species of strepsirrhine primates (Galagidae, Cheirogaleidae) and three species of fruit bats (Pteropodidae). Microdissection and light microscopy were employed to identify support structures of the orbit. In bats and primates, there are two layers of fascial sheets that border the eye laterally. The outer membrane is the most superficial layer of deep fascia, and has connections to the POB in primates. In fruit bats, which lacked a POB or analogous ligament, the deep fascia is reinforced by transverse ligaments. Bats and primates have a deeper membrane supporting the eye, identified as the periorbita (PA) based on the presence of elastic fibers and smooth muscle. The PA merges with periostea deep within the orbit, but has no periosteal attachment to the POB of primates. These findings demonstrate that relatively big eyes can be supported primarily with fibrous connective tissues as well as the PA, in absence of a POB or ligament. The well-developed smooth muscle component within the PA of fruit bats likely helps to protrude the eye, maintaining a more convergent eye orientation, with greater overlap of the visual fields. The possibility should be considered that early euprimates, and even stem primates that may have lacked a POB, also had more convergent eyes than indicated by osseous measurements of orbital orientation. Anat Rec, 299:1690-1703, 2016. © 2016 Wiley Periodicals, Inc., (© 2016 Wiley Periodicals, Inc.)

For nearly two decades, a database of brain structures from a large sample (272 species) of chiropterans has been widely accessible and used for socioecological analyses of mammals. However, this database remains incomplete since the hypophysis has not been measured. Since this glandular/neural structure has reproductive significance to chiropterans as for other mammals, this investigation was carried out using serial coronal sections of bat brains comprising the Heinz Stephan collection, Düsseldorf, Germany. Complete serially sectioned brains were examined in 313 individuals (165 species, 15 families). Using a well-documented method, hypophyseal volumes were determined from every fourth or sixth section in each individual. The strongest correlation was between body weight and the hypophysis (R(2) = 0.887) and its various components as well as between body weight and adenohypophysis (R(2) = 0.830) and neurohypophysis (R(2) = 0.925). Correlations were also strong for brain weight-adenohypophysis (R(2) = 0.817) and brain weight- neurohypophysis (R(2) = 0.911). Results indicated that: (1) in regression analyses, hipposiderids stand apart as having relatively large adenohypophysis; (2) analysis of residuals generated using least-squares regression of hypophyseal components suggests a trend among microchiropterans where females have a relatively larger adenohypophysis than males. However, this difference is only statistically significant in the largest samples: Phyllostomidae and Vespertilionidae. Pteropodids do not appear to follow this trend. Our findings suggest both phylogenetic and sexual differences in the adenohypophysis in particular, and indicate the need for investigation of larger samples by species, especially those best understood in reproductive and social biology., (© 2016 Wiley Periodicals, Inc.)

The olfactory recess (OR) is a restricted space at the back of the nasal fossa in many mammals that is thought to improve olfactory function. Mammals that have an olfactory recess are usually described as keen-scented, while those that do not are typically thought of as less reliant on olfaction. However, the presence of an olfactory recess is not a binary trait. Many mammal families have members that vary substantially in the size and complexity of the olfactory recess. There is also variation in the amount of olfactory epithelium (OE) that is housed in the olfactory recess. Among New World leaf-nosed bats (family Phyllostomidae), species vary by over an order of magnitude in how much of their total OE lies within the OR. Does this variation relate to previously documented neuroanatomical proxies for olfactory reliance? Using data from 12 species of phyllostomid bats, we addressed the hypothesis that the amount of OE within the OR relates to a species' dependence on olfaction, as measured by two commonly used neuroanatomical metrics, the size of the olfactory bulb, and the number of glomeruli in the olfactory bulb, which are the first processing units within the olfactory signal cascade. We found that the percentage of OE within the OR does not relate to either measure of olfactory "ability." This suggests that olfactory reliance is not reflected in the size of the olfactory recess. We explore other roles that the olfactory recess may play., (© 2014 Wiley Periodicals, Inc.)

The olfactory recess - a blind pocket at the back of the nasal airway - is thought to play an important role in mammalian olfaction by sequestering air outside of the main airstream, thus giving odorants time to re-circulate. Several studies have shown that species with large olfactory recesses tend to have a well-developed sense of smell. However, no study has investigated how the size of the olfactory recess relates to air circulation near the olfactory epithelium. Here we used a computer model of the nasal cavity from a bat (Carollia perspicillata) to test the hypothesis that a larger olfactory recess improves olfactory airflow. We predicted that during inhalation, models with an enlarged olfactory recess would have slower rates of flow through the olfactory region (i.e. the olfactory recess plus airspace around the olfactory epithelium), while during exhalation these models would have little to no flow through the olfactory recess. To test these predictions, we experimentally modified the size of the olfactory recess while holding the rest of the morphology constant. During inhalation, we found that an enlarged olfactory recess resulted in lower rates of flow in the olfactory region. Upon exhalation, air flowed through the olfactory recess at a lower rate in the model with an enlarged olfactory recess. Taken together, these results indicate that an enlarged olfactory recess improves olfactory airflow during both inhalation and exhalation. These findings add to our growing understanding of how the morphology of the nasal cavity may relate to function in this understudied region of the skull., (© 2014. Published by The Company of Biologists Ltd.)

The facial glands of bats are modified skin glands, whereas there are up to three different orbital glands: Harderian, lacrimal, and Meibomian glands. Scattered studies have described the lacrimal and Meibomian glands in a handful of bat species, but there is as yet no description of a Harderian gland in bats. In this study we examined serial sections of orbitofacial glands in eight families of bats. Much variation amongst species was observed, with few phylogenetic patterns emerging. Enlarged facial glands, either sudoriparous (five genera) or sebaceous (vespertilionids only) were observed. Meibomian and lacrimal glands were present in most species examined (except Antrozous), though the relative level of development varied. Two types of anterior orbital glands were distinguished: the Harderian gland (tubulo-acinar: observed in Rousettus, Atribeus, Desmodus and Miniopterus) and caruncular (sebaceous: observed in Eptesicus and Dieamus). The relative development of the nasolacrimal duct and the vomeronasal organ did not appear to be correlated with the development of any of the exocrine glands examined. There does, however, appear to be a correlation between the presence of at least one well developed exocrine gland and the level of communality and known olfactory acuity, best documented in Artibeus, Desmodus, and Miniopterus., ((c) 2010 Wiley-Liss, Inc.)

The vomeronasal organ (VNO) is known to be present in bats of the family Phyllostomidae, but in most species this is inferred from the presence of accessory olfactory bulbs. Like primates, bats have profound intergroup variations in the vomeronasal system. Of the family Phyllostomidae (49 genera, 143 species) the VNO of approximately 60 species has been studied. Here, we report light microscopic observations of the VNO of Anoura geoffroyi (fetus and adult), A. caudifer, and A. cultrata, as well as ultrastructural observations of the VNO in adult A. geoffroyi. The organ is crescent-shaped, with a wide lumen encroached by a "mushroom body" that contains a venous sinus. In adults, the vomeronasal cartilage is reduced, being longer in absolute length in fetal A. geoffroyi compared with the adult. In the neuroepithelium, the receptor cell microvilli are dark, distinct, and short, emerging from a vesicular tuft; the supporting cell microvilli are relatively much longer. Large paravomeronasal ganglia are observed. The receptor-free epithelium is undulating and lacks cilia or microvilli. Some characteristics of the VNO in Anoura have not been reported in other chiropterans to date, such as the marked reduction of the vomeronasal cartilage and absence of cilia in the receptor-free epithelium. Moreover, if A. geoffroyi is representative, the genus has an adult neuroepithelial volume similar to other mammals of its body size. Further examination of uninvestigated phyllostomid VNOs may elucidate a phylogenetic history of the family, as well as ecological or social correlates of the VNO in the order Chiroptera., (Copyright 2007 Wiley-Liss, Inc.)

The present study describes seasonal changes in delta5 3beta hydroxysteroid dehydrogenase (3beta-HSD), glusose-6 phosphates dehydrogenase (G-6-PD), and lipids in the ovary of a vespertilionid bat, Scotophilus heathi. Total lipids and 3beta-HSD activity are restricted to thecal and interstitial cells of the ovary. The total lipids, 3beta-HSD, and G-6-PD significantly increase during recrudescence, and remain high during winter dormancy and breeding as compared to the other reproductive phases. High incidence of lipids and enzyme activity in interstitial cells during the breeding period and at the time of ovulation clearly suggests that these cells are actively involved in steroidogenesis. A decline in enzymes and lipid activity during winter dormancy, which correlates with the declining levels of steroidogenesis, might be the factors responsible for prolonged survival of the Graafian follicle in the ovary of S. heathi.