Variability of Rheotaxis Behaviors in Larval Bullfrogs Highlights Species Diversity in Lateral Line Function

Abstract

The morphology and distribution of lateral line neuromasts vary between ecomorphological types of anuran tadpoles, but little is known about how this structural variability contributes to differences in lateral-line mediated behaviors. Previous research identified distinct differences in one such behavior, positive rheotaxis towards the source of a flow, in two tadpole species, the African clawed frog (Xenopus laevis; type 1) and the American bullfrog (Rana catesbeiana; type 4). Because these two species had been tested under different flow conditions, we re-evaluated these findings by quantifying flow-sensing behaviors of bullfrog tadpoles in the same flow field in which X. laevis tadpoles had been tested previously. Early larval bullfrog tadpoles were exposed to flow in the dark, in the presence of a discrete light cue, and after treatment with the ototoxin gentamicin. In response to flow, tadpoles moved downstream, closer to a side wall, and higher in the water column, but they did not station-hold. Tadpoles exhibited positive rheotaxis, but with long latencies, low to moderate accuracy, and considerable individual variability. This is in contrast to the robust, stereotyped station-holding and accurate rheotaxis of X. laevis tadpoles. The presence of a discrete visual cue and gentamicin treatment altered spatial positioning and disrupted rheotaxis in both tadpole species. Species differences in lateral-line mediated behaviors may reflect differences in neuromast number and distribution, life history, or perceptual salience of other environmental cues.

Ecological predictors of lateral line asymmetry in stickleback (Gasterosteus aculeatus)

“…Lateral line morphology, whether it be neuromast counts, pattern or internal structure, is highly variable among species due to its diversity of functions (Coombs et al 2014;Schmitz et al 2014). Many life history traits are associated with the lateral line, such as predator prey interaction (Coombs and Patton 2009;Junges et al 2010;Schwalbe et al 2012), rheotaxis (Baker and Montgomery 1999;Suli et al 2012;Brown and Simmons 2016;Jiang et al 2017), schooling (Middlemiss et al 2017;Mekdara et al 2018) and conspecific interaction (Butler and Maruska 2016). There is also a growing body of evidence showing that lateral line morphology is variable within species, particularly among populations in different habitats (Wark and Peichel 2010;Trokovic et al 2011;Fischer et al 2013;Planidin and Reimchen 2019).…”

Tadpole bioacoustics: Sound processing across metamorphosis.

“…In all flow conditions, bullfrog tadpoles exhibit long response latencies (up to 300 s). They do not station hold but continue to swim, although within a more localized area, when flow is present, and the precision of their orientation response (the vector strength) is significantly less than in African clawed frogs (Brown & Simmons, 2016; Figure 7).…”

“…There are considerable differences between tadpole species in the numbers and spatial distribution of neuromasts, related to the animal’s ecology and life history (Brown & Simmons, 2016; Hoff et al, 1999; Lannoo, 1987; Quinzio & Fabrezi, 2014). These differences likely reflect the importance of sensory input from the lateral line in guiding behavior.…”

“…It is a stereotyped and robust response (Figure 8; Simmons et al, 2004, 2015). Conversely, bullfrog tadpoles tested under the same flow conditions are more randomly oriented, and their responses are more affected by the specific flow dynamics of the testing tank (Brown & Simmons, 2016; Schmidt et al, 2011). In some flow conditions, these tadpoles swim away from, rather than toward, the source of the current.…”

“…African clawed frog tadpoles show greater precision of rheotaxis than do bullfrog tadpoles. Figure is modified from Brown and Simmons (2016).…”