Stress and dominance in a social fish

Abstract

Many aspects of reproductive physiology are subject to regulation by social interactions. These include changes in neural and physiological substrates of reproduction. How can social behavior produce such changes? In experiments reported here, we manipulated the social settings of teleost fish and measured the effect (1) on stress response as reflected in cortisol production, (2) on reproductive potential as measured in production of the signaling peptide, gonadotropin-releasing hormone, and (3) on reproductive function measured in gonad size. Our results reveal that the level of the stress hormone cortisol depends critically on both the social and reproductive status of an individual fish and on the stability of its social situation. Moreover, the reproductive capacity of an individual fish depends on these same variables. These results show that social encounters within particular social contexts have a profound effect on the stress levels as well as on reproductive competence. Social behavior may lead to changes in reproductive state through integration of cortisol changes in time. Thus, information available from the stress pathway may provide socially relevant signals to produce neural change.

Fig. 1.

Schematic representation of three experimental groups, showing relative tank dimensions and densities of T and NT males. A, Social pairs; B, high-density community tank; C, low-density community tank with under-gravel feeding via substrate tubing. The ratio of males to females (not shown) in each tank was 1:2 (community settings) or 1:3 (social pairs).

Fig. 2.

The stress response as measured by serum cortisol levels in Haplochromis burtoni as a function of time after onset of the stressor, which was removal of aquarium lid. Until 4 min after stress onset, cortisol levels remain below basal levels of 5.0 ng/ml. After this time, cortisol concentration rises substantially, suggesting that additional cortisol synthesized in response to the stress of capture. Accordingly, only blood collected within 4 min of aquarium lid removal was used for analysis. Differing cortisol levels in fish sampled within the first 4 min also highlight the divergent experiences of individuals during the previous 30 min of social interactions. Indeed, it is extremely difficult to obtain true basal levels of cortisol, because the fish are constantly interacting, and even social isolation has been shown to be stressful (Pottinger, 1992).

Fig. 3.

irGnRH soma sizes, corrected for body size, are shown for T and NT males in all three social settings studied. In all experimental groups, soma sizes are significantly smaller for NTs (open bars) than for Ts (striped bars) (p < 0.002 for social pairs;p < 0.01 for community settings; Student’st test). Error bars represent SEM.

Fig. 4.

Cortisol levels of NTs (open bars) and Ts (striped bars) shown for (A) low-density communities and (B) high-density communities (averaged). In both cases, the stability index (Δ) (see Materials and Methods) is superimposed on cortisol level data. In the low-density setting, differences in cortisol levels are plotted over the course of 7 weeks. High-density communities had been established for 2 months before blood sampling and are fully stabilized.

Fig. 5.

Cortisol levels in individual fish that switched social status. A, Single switches from T to NT;B, single switches from NT to T; C, multiple switches (note different ordinate scale in C). Fish had significantly higher cortisol levels as NT than as T (p < 0.05; Wilcoxon signed rank, using last switch if multiple switches per fish).