Calcification of the lower respiratory tract in relation to flight development in Jamaican fruit bats (Phyllostomidae, Artibeus jamaicensis)

Abstract

The production of echolocation calls in bats along with forces produced by contraction of thoracic musculature used in flight presumably puts relatively high mechanical loads on the lower respiratory tract (LRT). Thus, there are likely adaptations to prevent collapse or distortion of the bronchial tree and trachea during flight in echolocating bats. By clearing and staining (Alcian blue and Alizarin red) LRTs removed from nonvolant neonates, semivolant juveniles, volant subadults, and adult Jamaican fruit bats (Artibeus jamaicensis), I found that calcification of the tracheal, primary bronchial, and secondary bronchial (lobar) cartilage rings occurs over the span of about 3 days and coincides with later developmental stages of flight and the increased production of echolocation calls. Tracheal rings that are immediately adjacent to the larynx calcified first, followed by more caudal tracheal rings and then the rings of the primary and secondary bronchi. I suggest that calcification of LRT cartilage rings in echolocating bats provides increased rigidity to counter the thoracic compressions incurred during flight. Calcification of the LRT rings is an adaptation to support the emission of laryngeally produced echolocation calls during flight in bats.

Keywords: bats; bronchi; calcification; trachea.

Figure 1

Diagrams showing sagittal (A,C) and transverse (B) sections of a bat. Sections show the relationship of flight, flank, and the transverse thoracis muscles and hypothetical forces produced by these muscles (arrows pointing inward) during the generation of thoracoabdominal pressure. Stippling represents abdominal and thoracic body cavities and hatching represents the muscles. In the flying bat (A) the arrows indicate direction of the forces imposed by the pectoralis and flank muscles during the production of sonar. (B) Relationship of the transverse thoracis and pectoralis muscles. The transverse thoracis could compress the thoracic cavity during hanging which the pectoralis muscle would otherwise compress during flight. In the hanging bat (C) forces produced by the flank muscles could dissipate (outward pointing arrow) due to the absence of flight muscle contraction and a relatively unrestrained thoracic cavity. Contraction of the transverse thoracis could counteract this dissipation by helping restrain the thoracic cavity (from Lancaster et al. 1995 with permission).

Figure 2

Cleared and stained LRTs and intact larynges of Artibeus jamaicensis. Ages and flight stages are as follows: (A) flutter at 8 days old, (B and C) in the flight stage and both at 37 days old, showing the progression of calcification in a cranial to caudal direction, and (D) flight at 54 days. Uncalcified cartilage is stained blue and calcified cartilage red. Graduations represent 1 mm.

Figure 3

Percent of calcified tracheal rings plotted against age. Data points represent individual bats. ‘A’ represents individuals over the age of 106 days and deemed to be adults. Note rapid increase in percent of calcified rings between 36 and 38 days.

Figure 4

Bars represent average percentage of calcified tracheal rings for each flight stage. Error bar represents standard deviation; flight stages sharing the same letter are not statistically different from each other. Note that flutter, flap, and adult stages exhibited no variation.

Figure 5

Cleared and stained LRT from a 38‐day‐old individual. Caudal trachea and primary and secondary bronchi are shown. Graduations on the left represent 1 mm.

Figure 6

Cleared and stained LRT, larynx, and hyoid bone (stained red) from an adult lab mouse (Mus musculus). Graduations on the left represent 1 mm.