Brown EE and Simmons AM (2016), Variability of Rheotaxis Behaviors in Larval Bu...

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PLoS One 2016 Nov 07;1111:e0166989. doi: 10.1371/journal.pone.0166989.

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

Brown EE , Simmons AM .

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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.

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	Fig 1. XZ spatial position at different flow speeds in Experiment 1 (tadpoles tested in the dark).(A) Untreated tadpoles, X position. (B) Untreated tadpoles, Z position. Solid green bars show position in NF (No Flow) and solid blue bars show position in WF (With Flow). (C) Treated tadpoles, X position. (D) Treated tadpoles, Z position. Hatched green bars show position in NF and hatched blue bars show position in WF. All positions are shown as mean +/- standard deviation. The horizontal dashed line on each plot shows the midpoint of the tank in that dimension. Both untreated and treated tadpoles move towards the back of the tank in the X dimension (A,C) and farther up in the water column in the Z dimension (B,D).
	Fig 2. Changes in X position of individual tadpoles during NF and WF periods.(A) Untreated tadpoles. (B) Treated tadpoles. The NF period extends from 30 to 300 seconds and the WF period extends from 330 to 600 seconds. Flow is turned on at 300 seconds (vertical dashed line on each plot). Each colored line shows data from one tadpole at one flow speed. Tadpoles do not station hold in NF or in WF. Streamwise movements were reduced at a flow speed of 10 cm/s although crosswise movements still occurred. Tadpoles initiated movements within the first 30 second time interval after the flow is turned on, and change in movements were similar for untreated and treated tadpoles.
	Fig 3. Y positioning of individual tadpoles during NF and WF periods.(A) Untreated tadpoles. Each data point shows the mean Y position of one tadpole over the NF period (dark yellow circles) and over the WF period (dark red triangles). Data are not separated by flow speed, because data points overlapped substantially. Over all tadpoles, the mean Y position in NF is 7.2 and the mean Y position in WF is 7.6, as shown by the color-coded dashed lines. (B) Treated tadpoles. Data in NF are shown as dark yellow squares and data in WF are shown as dark red inverted triangles. The mean Y position in NF is 7.5 and the mean Y position in WF is 8.3, as shown by the color-coded dashed lines. Tadpoles are more clustered towards the middle of the tank in NF than in WF, with treated tadpoles positioned farther towards one side in WF.
	Fig 4. Orientation headings at different flow speeds in Experiment 1 (tadpoles tested in the dark).Circular plots (in degrees) showing orientation headings for untreated (A) and treated (B) tadpoles tested in NF (top row) and WF (bottom row) at different flow speeds (columns). The top NF plot (untreated, 2cm/s) shows the circular reference points (in degrees). The arrows on the left of the WF plots point to 0°, the crosswise midpoint of the source of the flow. An animal showing perfect positive rheotaxis would be oriented towards 0°. Red triangles (bin width of 5°) in each plot show the mean orientation, summed over ten time intervals (300 second total sampling time), of each individual tadpole. The length of the triangles indicates how many individual tadpoles exhibited that particular orientation. The numbers inside the circular plots in WF are the vector strengths of the orientation response. Results of the modified Rayleigh test (u, with corresponding P values) are shown below these plots. P values of 0.001 or below are statistically significant, according to our criterion. Statistical significance was not obtained in any NF condition.
	Fig 5. Spatial positioning in XZ dimensions in Experiment 2 (testing in the presence of a light cue).(A) Mean (+/- standard deviation) X positioning. (B) Mean (+/- standard deviation) Z positioning. Light location (upstream or downstream) and flow condition (NF, WF) are indicated on the x axis. In all plots, the dashed line shows the midpoint of the tank in that dimension. Untreated tadpoles are shown by the dark green bars and treated tadpoles are shown by the hatched dark blue bars. The presence and location of the light cue strongly affects positioning in the X dimension, while treatment affects positioning in the Z dimension.
	Fig 6. Orientation headings in Experiment 2 (testing in the presence of a light cue).Circular plots showing orientation headings of tadpoles tested in NF (top row) and WF (bottom row) in two light conditions (columns). Data are shown separately for untreated and treated animals. Tadpoles were not significantly oriented towards the location of the light cue (shown by the light symbol) or towards the source of the flow (in WF).
	Fig 7. DASPEI-stained neuromasts in bullfrog tadpoles.(A) Supra- and infra-orbital lines in an untreated stage 26 tadpole. Rostral is to the right. Scale bar = 1mm. (B) Composite of images from the tail of an untreated stage 25 tadpole. The trunk is to the left and the tip of the tail is to the right. (C) Supra- and infraorbital lines in a gentamicin-treated stage 26 tadpole. In all images, DASPEI fluoresces yellow. Images have been adjusted for brightness, contrast and color balance.
	Fig 8. Comparison of rheotaxis behaviors in bullfrogs (Rana catesbeiana) and African clawed frogs (Xenopus laevis).Tadpoles at comparable developmental stages were tested in the same flow tank at flow speeds of 2 and 4 cm/s. Black bars show data from bullfrogs and red bars show data from African clawed frogs. (A) Percent of animals showing significant positive rheotaxis. At both flow speeds, all African clawed frog tadpoles show rheotaxis, compared to a mean of 58% of bullfrog tadpoles. (B) Latency to achieve rheotaxis is longer in bullfrog tadpoles (mean of 183 seconds; including responses of animals that did not reach the criterion for rheotaxis) than in African clawed frog tadpoles (mean of 37 seconds). (C) Vector strength of the orientation response is higher in African clawed frog tadpoles (mean of 0.90) compared to bullfrog tadpoles (mean of 0.40).

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