Ultrastructure of the unusual accessory submandibular gland in the fringe-lipped bat,Trachops cirrhosus

Abstract

Background: The phyllostomid fringe‐lipped bat, Trachops cirrhosus, is sui generis (in a family of ca. 138 species) in that it subsists in part on tropical frogs. These amphibians frequently possess highly toxic integument. We examined the salivary glands of this bat to determine if these glands could be the source of protective factors that permit consumption of seemingly unsavory prey. The parotid and principal salivary glands of this bat are similar to homologous glands in other phyllostomids, but the accessory submandibular gland is unique. Methods The accessory submandibular glands of live‐trapped T. cirrhosus were fixed and processed for transmission electron microscopy by conventional means. Results The accessory submandibular gland consists of follicles and ducts. The principal cells of the follicular walls have an abundance of rough endoplasmic reticulum (RER), free ribosomes, and extensive Golgi apparatuses. Typically, these cells have relatively few serous secretory granules. The cells contain collections of peculiar lipid droplets, and some of their mitochondria have dense crystalloids within expanded cristae. A layer of irregular, moderately dense bodies lies immediately subjacent to the luminal plasmalemma; it is not clear if these structures are endocytotic or exocytotic. Clusters of mucous cells, some of which have a single, hugely distended RER cisterna, are ensconced in the follicular walls; mucus from these cells reaches the lumen via intercellular canaliculi. Ducts progress from simple cuboidal to simple columnar epithelium. They lack basal striations, and their constituent cells contain relatively few mitochondria. Follicles and ducts have numerous myoepithelial cells at their periphery, and both are heavily innervated by hypolemmal nerve terminals. Conclusions The unusual accessory submandibular gland in T. cirrhosus documents the extreme modifications in gland histology and in cell ultrastructure that have occurred in mammalian families. The cells composing the follicle walls and ducts bear little similarity to typical acinar or duct cells. Duplication of the submandibular gland in some bat lineages might be the key innovation underlying such plasticity. The heavy innervation of both follicles and ducts also implies that these structures are sensitive to and capable of responding to various inputs, perhaps including dietary factors. Anat. Rec. 248:164–175, 1997. © 1997 Wiley‐Liss, Inc.

Flexibility in assessment of prey cues: frog-eating bats and frog calls

“…T. cirrhosus also has tubercles on its chin and lips whose function is unknown but might allow chemosensory assessment of prey. If T. cirrhosus bites the prey, it may recognize unpalatable prey by taste, and for frog species that are only mildly poisonous, T. cirrhosus has specialized salivary glands that may reduce some of the toxins found in the frog's skin (Tandler et al 1997). The fact that T. cirrhosus does not have to rely solely on acoustic cues, but may also use additional means of prey assessment, increases the opportunity for flexibility in its assessment of prey cues.…”

“…The third peak is located in the apical portion of the cochlea, which is thought to detect lowfrequency sounds (Bruns et al 1989). In addition to its unusual low-frequency hearing, T. cirrhosus has unique salivary glands that may serve to neutralize toxins to allow the consumption of anuran prey (Tandler et al 1997).…”

An updated synthesis of and outstanding questions in the olfactory and vomeronasal systems in bats: Genetics asks questions only anatomy can answer

“…As these behaviors extend beyond the olfactory‐reliant pteropodids and phyllostomids, it suggests that chemical social communication in bats is widespread across most bat families. There are numerous reports of large sebaceous glands (Flores et al, 2019; Safi & Kerth, 2003; Scully & Fenton, 2000; Tandler et al, 1997), ranging from above the eyebrows, to the chest, to under the wing, which often have an unknown purpose; yet these large anatomical structures suggest that chemical secretions are somehow essential to the functional ecology of the animal.…”

Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat

“…T. cirrhosus, together with other frog-eating bats, possess unique accessory submandibular salivary glands, which may protect them from toxins and allow them to reject poisonous prey post-capture without ill effects (Tandler et al 1996(Tandler et al , 1997.…”