Behavioral ecology, endocrinology and signal reliability of electric communication

Abstract

The balance between the costs and benefits of conspicuous animal communication signals ensures that signal expression relates to the quality of the bearer. Signal plasticity enables males to enhance conspicuous signals to impress mates and competitors and to reduce signal expression to lower energetic and predation-related signaling costs when competition is low. While signal plasticity may benefit the signaler, it can compromise the reliability of the information conveyed by the signals. In this paper we review the effect of signal plasticity on the reliability of the electrocommunication signal of the gymnotiform fish Brachyhypopomus gauderio. We (1) summarize the endocrine regulation of signal plasticity, (2) explore the regulation of signal plasticity in females, (3) examine the information conveyed by the signal, (4) show how that information changes when the signal changes, and (5) consider the energetic strategies used to sustain expensive signaling. The electric organ discharge (EOD) of B. gauderio changes in response to social environment on two time scales. Two hormone classes, melanocortins and androgens, underlie the short-term and long-term modulation of signal amplitude and duration observed during social interaction. Population density drives signal amplitude enhancement, unexpectedly improving the reliability with which the signal predicts the signaler's size. The signal's second phase elongation predicts androgen levels and male reproductive condition. Males sustain signal enhancement with dietary intake, but when food is limited, they 'go for broke' and put extra energy into electric signals. Cortisol diminishes EOD parameters, but energy-limited males offset cortisol effects by boosting androgen levels. While physiological constraints are sufficient to maintain signal amplitude reliability, phenotypic integration and signaling costs maintain reliability of signal duration, consistent with theory of honest signaling.

Keywords: androgen; animal communication; cortisol; electric fish; melanocortin; signal plasticity; signal reliability.

Fig. 1.

Male and female electric organ discharge (EOD) in Brachyhypopomus gauderio. The male EOD (bold line) is greater in amplitude and longer in duration than the female EOD (thin line). The amplitude of the EOD predicts the body length of the signaler, while the duration of the EOD's second phase predicts androgen levels and reproductive condition.

Fig. 2.

Effect of androgens and cortisol on nighttime electric organ discharge (EOD) of Brachyhypopomus gauderio. 11-Ketotestosterone (11-KT) increases nighttime EOD amplitude (A), while both testosterone and 11-KT increase EOD duration (C) in comparison to blank implants (adapted from Goldina et al., 2011). In contrast, cortisol decreases both EOD amplitude (B) and EOD duration (D) in comparison to a control group treated with vehicle (adapted from Gavassa and Stoddard, 2012). Horizontal lines indicate group means while vertical lines indicate standard error of the mean. Significant differences between groups are indicated by lowercase letters.

Fig. 3.

Information conveyed by the electric organ discharge (EOD) in Brachyhypopomus gauderio. (A) The amplitude of the EOD predicts body length in both sexes. Data are shown from the sampling date with the highest population density (adapted from Gavassa et al., 2012b). (B) The duration of the EOD (τ_P2) predicts reproductive condition [gonadosomatic index (GSI)] in males. Moreover, EOD duration also predicts circulating levels of testosterone (C) and 11-ketotestosterone (D) in both sexes (adapted from Gavassa et al., 2011).

Fig. 4.

Signal reliability increases with population density in Brachyhypopomus gauderio observed in the field (A) and experimentally manipulated in the laboratory (B). R² values were obtained from the linear regression between body length and the natural logarithm of EOD amplitude [reprinted from Animal Behaviour, 83, Gavassa, S., Silva, A. C., Gonzalez, E. and Stoddard, P. K., Signal modulation as a mechanism for handicap disposal, 935-944, Copyright (2012), with permission from Elsevier].

Fig. 5.

Effect of food restriction and social treatment on the electric organ discharge (EOD) and circulating levels of 11-ketotestosterone in Brachyhypopomus gauderio. Social stimulation increases EOD amplitude (A) and duration (B); however, fish under food restriction (FR) increase both parameters more than fish on an ad libitum (AL) diet. Likewise, 11-ketostestosterone levels increase with social stimulation (C) (adapted from Gavassa and Stoddard, 2012).