Flow sensing in developing Xenopus laevis is disrupted by visual cues and ototoxin exposure

Abstract

We explored how lateral line cues interact with visual cues to mediate flow sensing behaviors in the nocturnal developing frog, Xenopus laevis, by exposing animals to current flows under different lighting conditions and after exposure to the ototoxin gentamicin. Under dark conditions, Xenopus tadpoles move downstream at the onset of current flow, then turn, and orient toward the direction of the flow with high accuracy. Postmetamorphic froglets also exhibit positive rheotaxis but with less accuracy and longer latency. The addition of discrete light cues to an otherwise dark environment disrupts rheotaxis and positioning. Orientation is less accurate, latency to orient is longer, and animals do not move as far downstream in the presence of light. Compared with untreated tadpoles tested in the dark, tadpoles exposed to gentamicin show less accurate rheotaxis with longer latency and do not move as far downstream in response to flow. These effects are compounded by the presence of light cues. The disruptive effects of light on flow sensing in Xenopus emphasize the disturbances to natural behaviors that may be produced by anthropogenic illumination in nocturnal habitats.

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

“…How ecological and morphological differences translate into behavioral differences in lateral line function has not been fully explored. Quantitative analyses of flow sensing behaviors in anurans have been limited to two species, the African clawed frog, Xenopus laevis (type 1), during larval and adult stages [6–13] and the bullfrog, Rana (formerly Lithobates ) catesbeiana (type 4), during larval stages [14]. Tadpoles of these two species differ in their propensity to exhibit rheotaxis, a standard metric of lateral line function which in fishes is mediated by superficial neuromasts [1,15].…”

“…X . laevis tadpoles show robust positive rheotaxis (orientation towards the direction of the flow source) [12,13] while bullfrog tadpoles of comparable developmental stages are more randomly and more variably oriented [14]. These differences in behavior may arise from several variables related to ecomorphological type, including neuromast organization, ecologies, foraging and predator avoidance behaviors, and life history.…”

“…In this experiment, we test this hypothesis by examining flow sensing behaviors of bullfrog tadpoles in the same flow field as used previously with X . laevis [13]. We also examine the impact on rheotaxis of two additional experimental manipulations—the presence of visual cues and treatment with gentamicin, an ototoxin that can damage neuromasts [1].…”

“…Discrete visual cues disrupt rheotaxis in larval X . laevis [13]; the influence of vision on rheotaxis in fishes varies with species, but in some testing conditions can guide, rather than disrupt, orientation behaviors [1, 16–19]. Gentamicin administration disrupts rheotaxis in larval X .…”

“…Gentamicin administration disrupts rheotaxis in larval X . laevis [13] as well as in fishes [20,21]. Combining these manipulations allows us to assess the salience of visual cues on rheotaxis both when the lateral line is functioning and when it has been damaged.…”