The African Cichlid Fish Astatotilapia burtoni Uses Acoustic Communication for Reproduction: Sound Production, Hearing, and Behavioral Significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2–5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes

Correlations between auditory evoked potential hearing threshold, circulating sex steroid levels, and gonadosomatic index (GSI) in the African cichlid fish <i>Astatotilapia burtoni</i>.

<p>11-KT, 11-ketotestosterone; E₂, 17β-estradiol; T, testosterone; <i>r</i>, correlation coefficient; <i>p</i><0.05 are in bold.</p

Summary of characteristics of courtship sounds produced by dominant male <i>Astatotilapia burtoni</i>.

<p><i>N</i>, number of animals; <i>n</i>, number of sounds or pulses analyzed.</p

Example of auditory evoked potential (AEP) traces recorded from <i>A. burtoni</i>.

<p>Averaged AEP traces from a representative subordinate male in response to a 200 Hz stimulus at several different intensities. An averaged trace from a control dead fish at 120 dB in response to a 200 Hz stimulus shows no response. Bottom trace shows the actual stimulus waveform recorded by the hydrophone at the position of the fish head. Threshold at this frequency was 105 dB_rms re: 1 µPa based on the repeatable waveform and the presence of an FFT peak at twice the stimulus frequency.</p

Characteristics of courtship sounds produced by male <i>A. burtoni</i> during quiver behaviors.

<p>A) Relationship between mean peak frequency (Hz) of sounds and male body size (standard length) shows that larger males produce lower frequency sounds. Each point represents the mean±SE of several sounds produced by an individual fish. B) There is a positive linear relationship between the number of pulses per sound and total sound duration (ms).</p

Dominant male <i>A. burtoni</i> produce intentional sounds during courtship quivers.

<p>A) Examples of the temporal sequence of courtship sounds and quiver behaviors produced by two individual males of different sizes. Top graph shows a small male (SL = 55 mm) that produced courtship sounds during ∼40% of behavioral quiver displays, while the bottom graph shows a larger male (SL = 82 mm) that produced sounds during ∼80% of quivers. Each vertical mark represents a single courtship sound or quiver behavior during the 30 min trial. B) Relationship between the percentage of quiver behaviors associated with courtship sounds and male standard length (SL) shows that larger males produce a greater proportion of behaviors with sounds than do smaller males.</p

Hearing thresholds in the cichlid fish <i>A. burtoni</i>.

<p>A) Hearing thresholds for subordinate and dominant males show similar responses, but subordinate males had lower thresholds at 600–800 Hz. B) Hearing thresholds for females show that receptive gravid individuals have lower thresholds at low frequencies from 100–600 Hz compared to mouthbrooding females. Threshold data are plotted as mean±SE (left axis). Asterisks indicate statistical differences between reproductive states within a sex at each test frequency (<i>p</i><0.05). Gray overlay lines represent the power spectra (128 point FFT, Hanning window) of a representative courtship sound and are plotted as relative amplitude in dB (right axis) for comparison of sound spectral energy to hearing thresholds. <i>N</i> = 8 fish for each reproductive state (for females) and social status (for males).</p

Dominant male <i>Astatotilapia burtoni</i> produce pulsed sounds during courtship quiver behaviors towards females.

<p>A) Photograph of a yellow dominant male in front of his pot territory performing a quiver display and courtship sound while presenting his anal fin egg-spots (arrow) towards two nearby, and attentive, gravid females. H, hydrophone. B) Representative waveform (top) and spectrogram (bottom) of a pulsed broadband courtship sound produced by a dominant male.</p