Venous networks in the upper airways of bats: A histological and diceCT study

Abstract

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.

The nasopharynx as a window to half a billion years of evolutionary change to the upper respiratory tract

“…Within the chiropteran sample, they compared nonecholocating bats with oral and nasal emitters of echolocation sounds. Although the study did not link the vascular mucosa to specializations of echolocation behaviors, Smith et al (2022, this volume) were able to quantify mucosal patterns between species in specific areas of interest such as the nasopharyngeal wall versus nasal cavity regions between hipposiderids and phyllostomids. It was found that, despite both hipposiderids and phyllostomids being nasal emitters of echolocation, the former have more numerous and widespread venous sinuses whereas the latter had mucosa that is not as well vascularized.…”

“…One of the many adaptations of bats includes the ability to hunt and navigate using echolocation. While some have studied skeletal adaptations for echolocation in the nasal cavities and upper airways of bats (Curtis et al, 2020; Curtis & Simmons, 2017), Smith et al (2022, this volume) focus on soft tissues of the noses and nasopharynges of several bat species, specifically epithelial distribution and the presence of subepithelial venous sinuses. They use diffusible Iodine‐based Contrast‐enhanced CT (diceCT) in conjunction with traditional histology to provide a fascinating analysis of two different methods for analyzing the presence of submucosal blood sinuses in the nasal cavities of bats.…”

“…Results suggest that the vascular mucosa of bats may serve a critical role in air‐conditioning and even at times with vomeronasal function rather than sound emission. Smith et al (2022, this volume) also provide evidence that dice‐CT can indeed be used for analyses that, traditionally, could only be performed via histology. This could allow for the processing of a greater number of specimens in a shorter amount of time and makes possible the mapping of venous sinuses and epithelial type over the entire upper respiratory tract.…”

The development of nasal turbinal morphology of moles and shrews

“…Mammals have plate-like structures called turbinals in the nasal cavity which possess bony or cartilaginous plate-like structures inside them (Moore 1981;Smith et al 2015;Smith et al 2021a). The turbinal expands the surface area in the nasal cavity by complex branching and scrolling (Parker 1874;Parker 1885;Martineau-Doizé et al 1992;Smith et al 2021aSmith et al , 2021b. Depending on their localization, the tissue on the surface of the turbinal is characterized by a large number of secretory goblet cells and capillaries and olfactory receptors (Negus 1958;Smith et al 2021b).…”

“…The turbinal expands the surface area in the nasal cavity by complex branching and scrolling (Parker 1874;Parker 1885;Martineau-Doizé et al 1992;Smith et al 2021aSmith et al , 2021b. Depending on their localization, the tissue on the surface of the turbinal is characterized by a large number of secretory goblet cells and capillaries and olfactory receptors (Negus 1958;Smith et al 2021b). Therefore, the turbinals have functions, such as warming the air from the outside world and absorbing water from the exhaled breath, and a role in olfaction (Negus 1958;Hillenius 1992).…”