Why Does the Male Goby Sing? By Don Orth

Do you now why the male goby sings?

We sometimes encounter two very similar fish species in similar places. When the two species are difficult for the novice to differentiate, we further wonder “How are the species reproductively isolated?”  Ernst Mayr, a leading evolutionary biologist of the 20^th century, classified reproductive isolating mechanisms into pre-zygotic (act before fertilization) and post-zygotic (act after fertilization).  In the case of sympatric species, behavioral isolation may involve distinctive behaviors designed to increase contact between breeding individuals of the same species. Post-zygotic mechanism are less efficient for reproductive isolation.  Although, we don’t often observe these isolating behaviors, there must be some subtle cues present during breeding.   Fish use pheromones (smell), vision, and sound for species recognition and reproductive isolation. Yes, fish make sounds that travel well underwater. We’ve known this for a long time (Myrberg et al. 1965; Gerald 1971).  Listen to a few fish making sounds here.

Reported maximum detection or propagation distances of mating sounds for (a) goby Gobiidae, (b) Oyster Toadfish Opsanus tau, (c) Bicolor Damselfish Stegastes partitus, and (d) Black Drum Pogonias cromis (Amorim et al. 2015).

Recent studies confirm that many fish species communicate via sound during courtship. Typically these are low-frequency sounds produced by males when close to females, while other fish make long-distance sounds to advertise their location. Black Drum Pogonias cromis can communicate up to 30–100 m (Amorim et al. 2015).  Goby males emit sounds from their nests to attract mates (Malavasi et al. 2008). It may not sound like singing to humans. But the male fish sings in order to attract a mate. There is enough information in the sound signals that the female can assess size and condition of potential mates.  In a recent paper, Eva-Lotta Blom and coauthors studied two species of gobies (Gobiidae) to examine visual and auditory cues during courtship. Two species, Common Goby Pomatoschistus microps and the Sand Goby Pomatoschistus minutus, are members of the species-rich family Gobiidae.  Gobies are small, benthic fishes with modified pectoral fins fused together, two dorsal fins, and often distinctive color patterns. Many are popular aquarium specimens favored for their colorful patterns or behaviors. See gallery of gobies. 

The Common Goby and the Sand Goby have sympatric distributions. During breeding they are found in close proximity, often competing over the same nest resources. To study the role of vision and sound in reproductive isolation, Blom and coauthors simultaneously recorded sounds with a hydrophone and visuals with a camcorder of breeding individuals under controlled lab conditions. What they learned was that females like males that sing.  In addition, there were visual cues that differed between species so that a female Common Goby would not be fooled by the behaviors of a male Sand Goby. 

 Common Goby (left, by Michel Barrabes) and Sand Goby (right, by Mazzun Tar-Ramel)

Differences in courtship behaviors and cues also help explain why the two morphologically and ecologically similar species select different habitats for breeding.  The courtship sound of the male Common Goby has shorter duration than the one of the Sand Goby.   Male Common Goby swim faster than male Sand Goby during courtship displays.  Finally, only the female Sand Goby display black eyes during courtship.   Nests of Common Gobies are more prevalent in shallow, soft bottom areas whereas Sand Goby nests use Mya clams in deeper, sandy beaches. The habitat differences influence sound transmission.

Oscillograms of representative sounds illustrate the distinctness of sounds of (A) male Common Goby and (B) male Sand Goby.  (Blom et al. 2016)

During breeding, visual cues are typically expressed by males as breeding coloration.  In the Sand Goby, the female display of black eyes acts as a declaration of intent that the female is ready to mate. Female Sand Gobies are able to change eye coloration, sometimes gradually, other times quickly, even within seconds.   The black eyes are not conspicuous in males.  In experimental aquaria, Olsson et al. (2017) observed that occurrence of female displaying dark eyes are more likely in those females close to spawning readiness, as measured by body roundness.

Bar chart illustrating the relationship between female roundness and frequency of dark eyes (black line). Frequency of dark eyes are illustrated in dark grey bars.   (Olsson et al. 2017).

As the studies of gobies illustrate, females prefer males that sing and can distinguish sounds for closely related species in order to isolate species reproductively.  The study raises questions about how males learn to sing and whether and how noise from human activities affect signals during breeding.   But now  you know why the male goby sings.

References

Amorin, M.C.P., R.O. Vasconcelos, and P.J. Fonsesa. 2015.  Pages 1-33 in F. Ladich, editor.  Sound Communication in Fishes.  Springer.

Blom,E-L., I. Mück, K. Heubel and O. Svensson. 2016. Courtship sound and associated behaviours of two sympatric marine Gobiidae species – Pomatoschistus microps and Pomatoschistus minutus. Environmental Biology of Fish 99: 999–1007.

Gerald, JW.1971. Sound production during courtship in six species of sunfish (Centrarchidae). Evolution 25:75–87.

Malavasi S, S. Collatuzzo, and P. Torricelli. 2008. Interspecific variation of acoustic signals in Mediterranean gobies (Perciformes, Gobiidae): comparative analysis and evolutionary outlook. Biological Journal of the Linnean Society 93:763–778.

Myrberg AA Jr, E. Kramer E, and P. Heinecke. 1965. Sound production by cichlid fishes. Science 149:555–558.

Olsson, K.H., S. Johansson, E-L. Blom, K. Lindström, O. Svensson, H. Nilsson Sköld and C. Kvarnemo. 2017. Dark eyes in female sand gobies indicate readiness to spawn. PLoS One 12: e0177714  http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0177714

Acoustics in Cichlid Reproductive Behavior, by Kyle Sullivan

Reproduction in fish is dependent on a large number of complex communication factors. The response of the female to male courtship behavior is largely based on the male’s identity, quality, motivation, readiness, and social status. Visual communication, the most studied and best understood mechanism, is just one of the multiple reproductive sensory mechanisms involved in reproduction. . Female choice often relies on visual traits such as size, dominance, mechanoreception, and chemoreception.  In Burton's Mouthbrooder Astatotilapia burtoni  (Günther, 1893), the male does  series of tail waggles that females use as an indicator of their dominance in the  social hierarchy.  Females also choose to reproduce with the male based on the acoustic frequency in combination with a multitude of other factors.

Soundwaves produced by a yellow dominant male during courtship (Maurska et al. 2012)

There are many factors that weigh into a female’s decision to reproduce with a male. Size is a contributor to female reception. A male displaying a certain trait that is larger (such as a larger caudal fin) may be more attractive in some species (Bischoff  et al. 1985). Some fish are considered dominant based on factors like size of territory owned or coloration. Dominant males are also more likely to reproduce (Spence 2006). Male odors can also influence a female's preference (Fisher et al. 2006). Females can also use their lateral line to either avoid males or court them (Medina et al. 2013).  The sexual response of a female Astatotilapia Burtoni is largely dependent on sounds produced by the male. Many fish use sound to deter predators and intruders, identify members of the same species, and to attract mates. Although the Astatotilapia Burtoni uses sounds in its courtship, it is important to note that not all fish, including many in the cichlidae family do not. Different sound frequencies may even influence morphological changes in some sympatric species, leading to reproductive isolation over time  (Longrie et al. 2013).

The likelihood that a female accepts a male as a mate is correlated with the frequency of the noise that he is emitting. These sounds are species specific, varying in “trill duration, number of pulses per trill, pulse period, pulse duration, and interpulse interval” (Maruska et al. 2012).  Females in the species Astatotilapia burtoni use sound to choose their mate based on frequency. This is tested in the paper written by Maruska, Ung and Fernald. The authors explain, “ we characterized the sounds and associated behaviors produced by dominant males during courtship, tested whether there were differences in hearing ability associated with female reproductive state or male social status, and then tested the hypothesis that female mate preference is influenced by male sound production.” (Maruska et al. 2012).

Astatotilpia burtoni has a brightly colored dominant male phenotype and a normal colored subordinate male phenotype. This makes them easy to distinguish and easier to use in experiments. The female’s response to courtship depends on the dominance of the male and the female’s reproductive potential at the time. Females that were mouthbrooding at the time were unlikely to respond to male courtship behavior. During courtship, males produce a low frequency sound when close to females. A female may respond to the male’s courtship differently based on the frequency of the noise produced. In the experiment from article one, the scientists used a tank with three compartments. They placed two visually and physically similar males on the outside compartments of the tank. They then introduced a female to the center compartment of the tank and played either the natural tail wag sound or the noise control from speakers in one of the outer compartments. When the natural sound was played through the speaker, the females spent a greater portion of their time on that side of the tank. When the unnatural control sound was played, the female spent equal amounts of time on either side of the tank. This suggests that females take into account acoustic signals when choosing a mate. It was determined that the tail wags are associated with courtship behavior, because “Dominant male A. burtoni produced pulsed broadband sounds during body quivers associated with courtship behaviors. Our simultaneous sound and video recordings demonstrate that these courtship sounds are produced intentionally because not all quiver behaviors were associated with sound production, suggesting that the sound is not merely a by-product of body movements, but that males have some control over when and where it is produced.” (Maruska et al. 2012).  The data show that the female prefers sounds produced by the male to be in a specific frequency threshold. More dominant males were able to produce sounds at the optimum hearing range and for a longer period of time. 

 The increase in the female sex steroid is correlated with the frequency of the sound produced by the male. According to Maruska, Ung, and Fernald, “Astatotilapia burtoni was most sensitive to low frequencies from ∼200–600 Hz, with a best frequency at 200–300 Hz, which overlaps the spectral content of the courtship sounds produced by dominant males.”  The sex steroids in the female increased when sounds in this range were played. When the steroids in the female are increased, the female is more likely to reproduce. The more dominant males are able to produce this sound while the less dominant males’ sounds are more likely to be ignored  (Maruska et al. 2012).

 

Larger males produce more sounds during courtship (Maruska et al. 2012)

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This research is a good indicator that, in combination with other traits such as size, dominance, mechanoreception and chemoreception, sound is used as a way to attract mates in the African Cichlid species Astatotilapia burtoni. During courtship, males produce courtship sounds that are conducive to increasing female sex steroids. This raises the female’s desire to mate with males who are more dominant, The experiment proved that the courtship sounds produced by Astatotilapia burtoni are both deliberate and vital to reproductive success.

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Bischoff, R. J., J. L. Gould, and D. I. Rubenstein. 1985.  Tail size and female choice in the Guppy (Poecilia reticulata).  Behavioral Ecology and Sociobiology   17(3):253-55.  doi:10.1007/bf00300143.
Fisher, H. S., B. B.m Wong, and G. G. Rosenthal. 2006. Alteration of the chemical environment disrupts communication in a freshwater fish.  Proceedings of the Royal Society B: Biological Sciences 273(1591): 1187-193. doi:10.1098/rspb.2005.3406.
Longrie, N., P. Poncin, M. Denoël, V. Gennotte, J. Delcourt, and E. Parmentier. 2013. "Behaviours Associated with Acoustic Communication in Nile Tilapia (Oreochromis niloticus)." PLoS ONE 8(4)  doi:10.1371/journal.pone.0061467.
Maruska, K. P., U. S. Ung, and R. D. Fernald.  2012.  The African Cichlid Fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance." PLoS ONE 7(5):e37612  doi:10.1371/journal.pone.0037612.
Medina, L.M., C.M. Garcia, A.F. Urbina, J.Manjarrez, and A. Moyaho. 2013. Female vibration discourages male courtship behaviour in the Amarillo Fish (Girardinichthys multiradiatus).  Behavioural Processes 100:163-68. doi:10.1016/j.beproc.2013.09.007.

Spence, R. 2006.   Mating preference of female Zebrafish, Danio rerio, in relation to male dominance.  Behavioral Ecology 17(5): 779-83.  doi:10.1093/beheco/arl016.