Semicircular canal size constrains vestibular function in miniaturized frogs

Abstract

Miniaturization has evolved repeatedly in frogs in the moist leaf litter environments of rainforests worldwide. Miniaturized frogs are among the world's smallest vertebrates and exhibit an array of enigmatic features. One area where miniaturization has predictable consequences is the vestibular system, which acts as a gyroscope, providing sensory information about movement and orientation. We investigated the vestibular system of pumpkin toadlets, Brachycephalus (Anura: Brachycephalidae), a clade of miniaturized frogs from Brazil. The semicircular canals of miniaturized frogs are the smallest recorded for adult vertebrates, resulting in low sensitivity to angular acceleration due to insufficient displacement of endolymph. This translates into a lack of postural control during jumping in Brachycephalus and represents a physical constraint resulting from Poiseuille's law, which governs movement of fluids within tubes.

Fig. 1.. Microcomputed tomography (microCT) imaging of the inner ear of Ischnocnema guentheri, B. brunneus, B. pernix, B. coloratus, and B. sulfuratus.

(Photographs by L.F. Ribeiro). The semicircular canals (SC) are oriented orthogonally to detect angular acceleration along three axes of motion (two vertical and one horizontal). Endolymph moves through the membranous duct within the semicircular canals. Lumen radius (r) was estimated as the distance from the outer margin of the endocast to the center of the endocast at its narrowest point (minimum circumference). This measurement represents the maximum possible value of r based on dimensions of the bony labyrinth, rather than the membranous duct which was unavailable. Circuit radius (R) was estimated by fitting a curve to a series of points placed along the midpoint of the entire canal (red dashed line) and measuring the distance to the center of the torus.

Fig. 2.. Log-log plot of lumen radius (r) versus circuit radius (R) for groups of adult and larval vertebrates [modified from (5)] with the canal dimensions of 147 anuran species superimposed.

Values for anurans, elasmobranchs, bony fish, and mammals represent means of the anterior, posterior, and lateral semicircular canals (2). Measurements for larval Xenopus and zebrafish are based on lateral canals only. Measurements for nonanuran miniaturized taxa were unavailable and are not included. Miniaturized and small-bodied frogs <24 mm (39) are represented by triangles. Ascaphus and Leiopelma are represented by stars. All other frogs are represented by circles. The dashed blue line is the regression line, R = 38.9 × r^1.60 estimated from a large sample of vertebrates (n = 285) (2).

Fig. 3.. Phylogenetic RMA regression of inner ear variables versus HW and SUL versus HW for 147 anuran species.

(A to G) Red line is the RMA regression line based on 100 alternative topologies. Blue line indicates simple isometry. (A) RLSC, circuit radius of lateral semicircular canal; (B) RASC, circuit radius of anterior semicircular canal; (C) RPSC, circuit radius of posterior semicircular canal; (D) rLSC, lumen radius of lateral semicircular canal; (E) rASC, lumen radius of anterior semicircular canal; (F) rPSC, lumen radius of posterior semicircular canal; (G) the two smallest miniaturized genera are represented by orange (Paedophryne) and red (Brachycephalus) circles. See Table 2 for scaling parameters.

Fig. 4.. Kinematic timing (in milliseconds) mapped onto a phylogeny of 23 anuran genera (48).

Phases included launch [beginning of movement (BM) to toe off (TO)], flight [TO to landing contact (LC)], landing [LC to end of forward progress (EFP)], and recovery [beginning of hindlimb flexion (HF) to end of movement (EM)]. Note the delayed hindlimb recovery in Brachycephalus, which does not begin until after EFP. The tree frog Phyllomedusa also exhibits a relatively long cycle duration. However, it uses derived landing behavior that involves stretching out the limbs to make better contact with adhesive toe pads (54). See data S4 for SDs.