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, 6 (5), e20313

Visual Information Alone Changes Behavior and Physiology During Social Interactions in a Cichlid Fish (Astatotilapia Burtoni)

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Visual Information Alone Changes Behavior and Physiology During Social Interactions in a Cichlid Fish (Astatotilapia Burtoni)

Chun-Chun Chen et al. PLoS One.

Abstract

Social behavior can influence physiological systems dramatically yet the sensory cues responsible are not well understood. Behavior of male African cichlid fish, Astatotilapia burtoni, in their natural habitat suggests that visual cues from conspecifics contribute significantly to regulation of social behavior. Using a novel paradigm, we asked whether visual cues alone from a larger conspecific male could influence behavior, reproductive physiology and the physiological stress response of a smaller male. Here we show that just seeing a larger, threatening male through a clear barrier can suppress dominant behavior of a smaller male for up to 7 days. Smaller dominant males being "attacked" visually by larger dominant males through a clear barrier also showed physiological changes for up to 3 days, including up-regulation of reproductive- and stress-related gene expression levels and lowered plasma 11-ketotestesterone concentrations as compared to control animals. The smaller males modified their appearance to match that of non-dominant males when exposed to a larger male but they maintained a physiological phenotype similar to that of a dominant male. After 7 days, reproductive- and stress- related gene expression, circulating hormone levels, and gonad size in the smaller males showed no difference from the control group suggesting that the smaller male habituated to the visual intruder. However, the smaller male continued to display subordinate behaviors and assumed the appearance of a subordinate male for a full week despite his dominant male physiology. These data suggest that seeing a larger male alone can regulate the behavior of a smaller male but that ongoing reproductive inhibition depends on additional sensory cues. Perhaps, while experiencing visual social stressors, the smaller male uses an opportunistic strategy, acting like a subordinate male while maintaining the physiology of a dominant male.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Sketch showing the aquarium used for the behavioral paradigm.
An experimental tank (45l.) was divided in half with a watertight, clear divider (gray mid-line) and a removable opaque barrier (black mid-line). The small male fish in the left compartment is the subject and the large male fish (∼ 4 times larger) in the right compartment is the stimulus. A half terra cotta pot was cut in half and placed so that both the stimulus and subject “shared” the same shelter (dark curve). Note that this “shared” shelter was hemisected by both center dividers. A layer of gravel covered the bottom of the tank and the dotted lines identify three zones in each compartment used to record animal position.
Figure 2
Figure 2. Bar graphs showing the mean dominance indices (DI) as a function of time.
The results shown are: before visual exposure (control) and after visual exposure for three groups of animals up to 1 day (A), up to 3 days (B) and up to 7 days (C). Seeing aggressive acts by the larger conspecific male continuously suppressed the dominant behavior of the subjects. The subjects had decreased dominance indices one hour after seeing the aggressive stimuli in all three groups. The solid bars are subjects that were exposed visually to the larger stimulus male and the hatched bars are control subjects that saw no other fish. Mean values with letters are significantly different from corresponding mean values without letters. The standard errors (SE) of means are shown as error bars.
Figure 3
Figure 3. Seeing the larger conspecific male caused the subject to abandon his territory in the shelter.
(A) The subjects reduced visits to the pot shelter (F(1, 380) = 13.535, p<0.001) and (B) reduced the percentage of time spent in the pot zone out of total observation time (F(1, 370) = 8.399, p = 0.004). Means with superscript letters are significantly different from those without letters. Error bars are the standard errors of means.
Figure 4
Figure 4. Circulating 11-KT concentrations were influenced by visual information and were correlated with dominant behaviors.
(A) The circulating 11-KT concentrations were suppressed in the first 24 hours by the stimulus, and increased after 3 days in the new environment. The bars show the mean 11-KT (± SE) of the subjects (solid) and the controls (hatched) at day 1 (D1), day 3 (D3) and day 7 (D7). (B) The mean DI (± SE) as a function of groups. D1: Day 1 group; D3: Day3 group; D7: Day7 group. Means with no common superscript letters are significantly different. The standard errors of means are shown as error bars. (C) The DI was positively correlated with plasma 11-KT levels (r = 0.509, p<0.001, n = 58). The black dots represent the subjects, and the white dots represent the controls.
Figure 5
Figure 5. The frequency of aggressive behaviors was correlated with androgen concentrations in the plasma.
The x-axis shows the frequency of all aggressive behaviors (chasing and border display). The T concentrations are shown on the left y-axis and were positively correlated with aggression (black circle; solid regression line; r = 0.384, p = 0.0438, n = 28). The 11-KT levels are shown on the right y-axis and were also positively correlated with aggression (gray triangles; dotted regression line; r = 0.506, p = 0.027, n = 19).
Figure 6
Figure 6. Brain gene expression levels were influenced by the visual stimulus after 3 days of exposure.
Expression of stress related mRNAs, including CRF (A), CRFBP (B) and AVT (E) changed significantly. (C) CRF-R1 expression levels decreased following onset of visual threats, but (D) CRF-R2 expression levels increased. (F–H) Expression of the three GnRH mRNA levels increased following onset of visual threats at day 3. Means with superscript letters are significantly different from those without letters. Error bars show the standard error of the mean.
Figure 7
Figure 7. The CRF, CRFBP, CRF-R1 and CRF-R2 expression levels were significantly correlated with the dominance index (DI).
(A) CRF and (B) CRF-R2 expression in the brains of experimental subjects was correlated with aggression (r = −0.562 and −0.584, p≤0.001, n = 29). (C) The total CRFBP expression levels were related to DI regardless of the visual experience (r = −0.278, p = 0.0347, n = 58). (D) In the control subjects, the CRF-R1 expression in the brain was related to dominance indices (r = 0.469, p = 0.0137, n = 27) and viewing the large conspecific male visually diminished this effect. The black dots represent the subjects, and the white dots represent the controls.

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