Exposure to agricultural pesticide impairs visual lateralization in a larval coral reef fish

Abstract

Lateralization, i.e. the preferential use of one side of the body, may convey fitness benefits for organisms within rapidly-changing environments, by optimizing separate and parallel processing of different information between the two brain hemispheres. In coral reef-fishes, the movement of larvae from planktonic to reef environments (recruitment) represents a major life-history transition. This transition requires larvae to rapidly identify and respond to sensory cues to select a suitable habitat that facilitates survival and growth. This 'recruitment' is critical for population persistence and resilience. In aquarium experiments, larval Acanthurus triostegus preferentially used their right-eye to investigate a variety of visual stimuli. Despite this, when held in in situ cages with predators, those larvae that previously favored their left-eye exhibited higher survival. These results support the "brain's right-hemisphere" theory, which predicts that the right-eye (i.e. left-hemisphere) is used to categorize stimuli while the left-eye (i.e. right-hemisphere) is used to inspect novel items and initiate rapid behavioral-responses. While these experiments confirm that being highly lateralized is ecologically advantageous, exposure to chlorpyrifos, a pesticide often inadvertently added to coral-reef waters, impaired visual-lateralization. This suggests that chemical pollutants could impair the brain function of larval fishes during a critical life-history transition, potentially impacting recruitment success.

Figure 1

Schematic representation of the test apparatus for eye lateralization determination. The three dark gray walls represent the opaque wall of the aquarium, while the light blue wall corresponds to the transparent wall where the visual stimuli are presented. No eye preference was recorded when the fish was perpendicular to the transparent wall (i.e. binocular stimulation) or when it formed an angle larger than 180° with respect to the transparent wall (i.e. fish looking in the opposite direction).

Figure 2

Left-right eye preference of A. triostegus larvae during the inspection of visual stimuli in an adjacent aquarium. Figure represents LI mean (±SE) values. Asterisks indicate significant differences (Mann-Whitney U tests, *p < 0.05; **p < 0.01) between Laterality Index (LI) values and the theoretical 50% value (dotted line). 13 to 14 replicates (one fish per replicate) were conducted for each visual stimulus.

Figure 3

Ecological importance of brain lateralization in larval survival facing direct predation. Survival index (SI) was calculated as follows: survival rate of the group minus the overall survival rate in the in situ cage. Figure represents SI mean ( ± SE) values. The asterisk indicates a significant difference in survival index among the three groups (Kruskal-Wallis test, x ² = 7.064, df = 2, p-value = 0.029) with ‘left-eye dominant’ experiencing higher survival than both ‘right-eye dominant’ (Nemenyi post-hoc test with Tukey-Dist approximation, p-value = 0.01) and ‘no eye dominant’ larvae (Nemenyi post-hoc test with Tukey-Dist approximation, p-value = 0.03). Six replicates were conducted. In each replicate, each group was made up with the same amount (four to six) of fish.

Figure 4

Effect of pesticides on the visual preference of A. triostegus larvae. Figure represents LI mean (±SE) values. Asterisks indicate significant differences (Mann-Whitney U tests, *p < 0.05; **p < 0.01) between Laterality Index (LI) values and the theoretical 50% value (dotted line). Black asterisks above bars indicate a significant right-eye preference, while white asterisks below bars indicate a significant left-eye preference. 10 to 11 replicates (one fish per replicate) were conducted for each visual stimulus in both the pesticide exposition experiment (black bars) and the solvent-control exposition experiment (grey bars).