Exposure to a nocturnal light pulse simultaneously and differentially affects stridulation and locomotion behaviors in crickets

Abstract

It is crucial for living organisms to be in synchrony with their environment and to anticipate circadian and annual changes. The circadian clock is responsible for entraining organisms' activity to the day-night rhythmicity. Artificial light at night (ALAN) was shown to obstruct the natural light cycle, leading to desynchronized behavioral patterns. Our knowledge of the mechanisms behind these adverse effects of ALAN, however, is far from complete. Here we monitored the stridulation and locomotion behavior of male field crickets (Gryllus bimaculatus), raised under light:dark conditions, before, during, and after exposure to a nocturnal 3-h pulse of different ALAN intensities. The experimental insects were then placed under a constant light regime (of different intensities); their behavior was continuously monitored; and the period of their daily activity rhythms was calculated. The light pulse treatment induced a simultaneous negative (suppressing stridulation) and positive (inducing locomotion) effect, manifested in significant changes in the average level of the specific activity on the night of the pulse compared to the preceding and the following nights. The transition to constant light conditions led to significant changes in the period of the circadian rhythms. Both effects were light-intensity-dependent, indicating the importance of dark nights for both individual and population synchronization.

Keywords: ALAN; Gryllus bimaculatus; artificial light at night; circadian rhythm; insect; light pollution; masking.

FIGURE 1

The experimental timeline: Adult, male crickets reared under LD 12:12 illumination regime (see Materials and Methods for details) were placed individually, each in an anechoic chamber, and their stridulation and locomotion monitored simultaneously (two left black boxes). On the night following three consecutive nights of consistent stridulation behavior, the experimental crickets were exposed to a light pulse (yellow box) of the duration of three hours and an intensity of 2, 5, or 40 lux. Following three to five additional nights under LD regime (right black box), the experimental animals were subjected to 12 h light:12 h ALAN (LA) or constant light (LL) conditions for at least five consecutive days and nights (grey box).

FIGURE 2

Double-plotted actograms representing light-pulse-dependent behavior of experimental crickets. Normalized activity of stridulation (orange) and locomotion (blue) are shown for each light intensity (A) 2 lux, (B) 5 lux, and (C) 40 lux. The first arrow and red rectangle represent the pulse treatment showing either a weak to no behavioral reaction (A, B), or a strong masking reaction to the light pulse (C). The general area of the plot around the time of the pulse was enlarged. The second arrow indicates the transition from LD into LA (constant, night-long ALAN) or LL (constant 40 lux), whereas nocturnal light intensity matched the pulse intensity. Yellow and black bars indicate diurnal and nocturnal phases, respectively.

FIGURE 3

Normalized mean level (±s.e.) of stridulation (A–C) and locomotion (E–G) behavior, three nights before (‘Pre’), during the pulse treatment (‘Pulse’, yellow), and three nights after (‘Post’) a pulse of 2 lux (A, E; n = 9), 5 lux (B, F; n = 8), and 40 lux (C, G; n = 8). (D–H) The normalized mean behavior levels (D, stridulation; and H, locomotion) during the pulse treatment under the different pulse intensities. *p < 0.05, **p < 0.01, ***p < 0.001.

FIGURE 4

Percentage of normalized level of (A) stridulation, and (B) locomotion behavior, one hour before (black), and one hour after (grey) the light pulse treatment of 2 lux, 5 lux, and 40 lux. *p < 0.05, **p < 0.01, representing one-tailed p-values.

FIGURE 5

The transition from LD to LA or LL affects the individual daily activity periods of stridulation (A) and locomotion (B) in a light intensity dependent manner. LD (before transition, black, n = 20), LA₂ lux (dark grey, n = 7), LA₅ lux (light grey, n = 7) and LL₄₀ lux (yellow, n = 6, n = 7 for stridulation and locomotion, respectively) treatments. *p < 0.05, **p < 0.01, ***p < 0.001.