Cichlidophiles: Can You Hear Me Now? Sound Production in Cichlid Courtship and Speciation
Author: Wayne S. Leibel
There are some estimated 600 distinct species of cichlids in Lake Malawi, one of the most dramatic examples known to biologists of explosive speciation and adaptive radiation that has occurred in vertebrates. (The cichlid flock of Lake Victoria is another.) Though the exact mechanism of their rapid speciation is not known, it is believed that the food- and niche-rich huge tropical African Rift Lakes provided the specialization/adaptive radiation (diversification) possibilities for ancestral cichlids, and the peculiar cichlid lifestyle and behavior provided the means. In particular, the combination of morphologically plastic pharyngeal jaws under genetic control that allowed for trophic specialization, along with the relatively complex reproductive behavior of cichlids (e.g., courtship, parenting, etc.), which allowed for quick genetic/reproductive isolation of new forms/species, are together responsible for this unique evolutionary phenomenon.
As the sometimes outrageous color patterns (which is certainly one of the reasons we keep them in our aquariums) of cichlids would indicate, color vision is an exceedingly important sensory modality for these highly social fish. Cichlids communicate their behavioral state—aggressive, amorous, fearful, parental, etc.—by changing their color patterns via innervation and hormones. Bands and spots appear and disappear as befits the situation, but the basic color pattern of a species is, well, species-specific and genetically determined. It is unique to that species and is believed to serve as a species recognition signal, primarily for females who are “choosy” in selecting males to breed with.
In polygamous cichlids like the ovophilus (immediate) mouthbrooders of Lake Malawi (the majority of species there), females tend to be plain, while the males are distinctively and often outrageously colored. In evolutionary parlance, these bright, species-specific male patterns are believed to have arisen via what Darwin called “sexual selection” in which choosy females select the best, most fit male for their sperm donor, and use color (principally brightness as a measure of health and nutritional state) as a means of choosing males of the right species and for evaluating their fitness. (The same story was offered by Darwin about the origin of the outrageous feathers of the male peacock.) Of course it helps if, as a male, you hold a territory to attract the female into to swap gametes, but often that too is a function of color in male-to-male competition and dominance.
Given the often reef-like environment of Lake Malawi, which teems with many species of cichlids swimming together, being able to quickly and accurately choose your own species (i.e., shared gene pool) is crucial; hybridization, either deliberate or by mistake, is usually a dead-end in the long run and strongly selected against. If the “species” have been genetically separated for a long period of time, chances are good that they no longer resemble each other to any great degree. However, for speciating (in process) or newly speciated, closely related species, the differences may not be that dramatic…yet. Evolution will make sure, by necessity, that they eventually will be, or hybridization will merge them into one. Whatever other signals help in the discrimination—subtle changes in courtship behavior, “smell” (yes, pheromones), even sound—will be selected for.
Although we are not used to thinking of cichlids as having a well-developed sense of hearing (and in fact hearing is a rather indirect process in fish compared to, say, mammals which have specialized hearing organs, e.g., “ears”), it is clear that some fish—including the marine damselfishes, near relatives of cichlids—do indeed use sound for communication, including species recognition (e.g., Myrberg, A. and J. Riggio, 1985. “Acoustically Mediated Individual Recognition by a Coral Reef Fish.” Animal Behaviour 33: 411-416; Spanier, E., 1979. “Aspects of Species Recognition By Sound in Four Species of Damselfishes.” Zeitschrift fur Tierpsychologie 51:301-316). It therefore becomes reasonable to ask whether cichlids can and do use sound for communication and species recognition.
Dr. Lobel’s Analysis
Dr. Phillip Lobel recently reviewed the relatively scant literature on this topic (2001. “Acoustic Behavior of Cichlid Fishes.” Journal of Aquaculture and Aquatic Sciences 9: 167-186). Lobel believes the mechanism of sound production in cichlids involves the jaw apparatus, with sounds amplified by the swimbladder. Indeed, a variety of sounds have been recorded from a number of cichlid species including Haplochromis burtoni (African riverine mouthbrooder), Hemichromis bimaculatus (African jewelfish), Herotilapia multispinosa (rainbow cichlid, Central America), Oreochromis mossambicus(Mozambique mouthbrooder), Simochromis babaulti and S. diagramma (Lake Tanganyika), Tropheus brichardi, T. duboisi, and T. moorii (Lake Tanganyika), and Copadichromis conophoros and Tramitichromis intermedius (Lake Malawi).
The Amorim Study
In a more recent article by Amorim and associates (Amorim, M., M. Knight, Y. Stratoudakis, and G. Turner, 2004. “Differences in Sounds Made by Courting Males of Three Closely Related Lake MalawiCichlid Species.” Journal of Fish Biology 65: 1358-1371) sounds from three Malawi mbuna are recorded and analyzed, and the results suggest that sound may play a larger role in cichlid species recognition than we thought.
In this study, three closely related species of the Pseudotropheus (now Maylandia) zebra complex were studied with regard to their courtship sounds. The three species were M. zebra, M. callainos, andM. sp. “zebra gold,” which differ strikingly in male courtship colors, but are very similar in other morphological traits.
As described by Amorim et al., M. zebra are pale blue with black vertical bars, males of the undescribed species M. sp. “zebra gold” have a similar pattern of brown bars on a yellow background, while M. callainos males are uniformly pale blue. The corresponding females of M. zebra and M. sp.“zebra gold” are very similar and easily confused, whereas M. callainos females are distinctively colored (blue or white). Previous genetic studies using microsatellite DNA markers show that these three species are reproductively isolated and that they mate assortatively (do not hybridize in a choice situation) in the laboratory. Thus, they are good, genetically differentiated species.
Three test aquaria (about 5 x 1½ x 2 feet), one per species, each divided into three approximately 20-inch-long compartments by two opaque, removable partitions, were used to test sound production. Seven or eight females of the tested species were maintained in the central compartment. Each end compartment held a single male and contained a clay pot as a refuge and spawning site. Males were introduced into the end compartments and visually isolated from the females in the middle until acclimatized, typically at least 24 hours. The opaque partition was then removed and any sounds each male made recorded with a sensitive hydrophone while their behaviors were observed so that particular sounds and behaviors could be paired. According to Amorim et al., male courtship behavior in all three species consists of a series of invariant movements/components that are not always displayed in a fixed order. These include “quiver” (male trembling in front of female); “dart” (male makes exaggerated but rapid 180-degree turns displaying opposite flanks in quick succession); “lead swim” (male flutters caudal and dorsal fins and attempts to lead female to the spawning site); “circle” (head to tail following in tight circles over the spawning site often culminating in spawning).
The recorded sounds were made up of repeated pulses which were further analyzed by digitization/computer sonograms and oscillograms (waveform displays) into five components: sound duration; time elapsed from the start of first pulse to end of last pulse; number of pulses; pulse period; pulse duration; and peak frequency. Differences among species in these five sound components were tested statistically, as were differences between individual males within a species. A total of 638 sounds were successfully recorded: 212 from 11 M. sp. “zebra gold,” 152 from 7 M. zebra, and 274 from 10 M. callainos males.
Twelve males neither attempted courtship nor produced any sound. Sound was produced by every male that attempted to court a female. The sounds emitted by the males of these three species had peak frequencies < 720 Hz, pulse durations of 9 to 12 milliseconds, a pulse period of 60 to 70 milliseconds, and sound duration varying between 500 to 700 milliseconds. To the untrained eye (mine) the sonograms and oscillograms do look slightly different, but in general are low frequency pulsed sounds and compare well with those from the other African cichlids already in the published literature (as above).
Courtship behavior and sound production were significantly related, with the majority of sounds being produced during the male “quiver” and “circling” displays. None of the five sound components differed significantly among males of the same species. However, there were significant differences among species in pulse duration and peak frequency. Maylandia callainos was the species most clearly distinguished based on sound properties, having a significantly higher peak frequency than M. sp. “zebra gold” and a significantly higher pulse duration than M. zebra. When Amorim et al. focused specifically on M. sp. “zebra gold” and M. callainos, the two species for which they had the most data (most recorded males), they also found a significant difference in the number of pulses between the two species.
Dr. Lobel’s 1998 Finding
In 1998, Lobel (“Possible Species Specific Courtship Sounds by Two Sympatric Cichlid Fishes in Lake Malawi Africa.” Environ. Biol. Fishes 52: 443-452), according to Amorim et al., had previously shown statistically significant differences in pulse rates and durations for two Malawian cichlids and proposed that courtship sounds could play a role in mate choice and species recognition. However, as Amorim et al. point out, the two species in that study, Copadichromis conophoros and Tramitichromis cf. intermedius, are not closely related, certainly not to the extent that the three species of Maylandiastudied here are.
As the authors point out, while their current results are tantalizing, it remains to be demonstrated whether cichlids—females of these cichlids in particular—can actually differentiate among males based on these courtship calls, as is the case for frogs and insects. Though Amorim et al. wisely choose to interpret their results conservatively, they suggest that courtship signals involving sensory modalities other than vision, including acoustic (sound) and possibly olfactory (smell) may well be involved in cichlid species recognition and mate choice, and may have contributed to cichlid speciation. These suggestions await experimental confirmation, but I won’t be surprised when it is demonstrated that female cichlids can and do choose mates on the basis not just of color, but also sound and smell.