Mating Systems and Parental Care in CichlidsAuthor: Samantha A. Hilber & Ronald M. Coleman
Fishes are an amazing group of animals in that for almost any mating or parental strategy that exists in the natural world, there is a species of fish that uses it. They are an incredibly diverse and behaviorally interesting group of animals. Cichlids provide the best opportunity to examine the evolution of parental care in fishes, as they show quite a bit of diversity in caring for their offspring.
The reproductive strategies of all fishes can broadly be broken up into two groups based on how egg fertilization occurs: internal fertilization versus external fertilization. This difference in fertilization has a huge impact on the mating and care strategies that can evolve.
In the typical system with internal fertilization, the male has a modified anal fin (called a gonopodium) that he uses to transfer sperm packages into the female. A male will use one of two basic strategies to mate with a female. He may court her with showy displays, or alternatively he may sneak up on her and insert sperm quickly before swimming away. Females may also court males occasionally.
Typically in these systems the parental strategy is female-only care. Maternal care in these fishes consists of the female retaining embryos within the body cavity until the offspring are fully developed and can swim and forage on their own. Guppies, mollies, and mosquitofish are examples of fishes that have this type of mating system and parental care.
In contrast to livebearers, most other fishes have external fertilization. This is when the female and the male release eggs and sperm into the environment. There is a lot of variation in exactly where and how external fertilizers release eggs and sperm. Many marine fishes, for instance, will swim up into the water column (often in groups) and release eggs and sperm at the same time, which then drift away. These species do not show any parental care. Many other fishes will place the eggs into a pre-constructed nest. At this point there are two distinct groups. In some species the male will exhibit territoriality, but he will not give any direct care to the young. In other species the male will also fan the eggs, remove dead eggs, and guard the nest against predation. It is thought that the presence of territoriality and nest construction are a precursor to the evolution of male parental care in fishes.
It is worth noting that when parental care is present in fishes it is typically male-only care. These males will hold a nest and receive eggs from multiple females. A female will usually give batches of eggs to several males, but may also give an individual male more than one batch of eggs. In such systems, fascinating alternative mating strategies may occur. For example, in bluegill sunfish there are three male mating strategies: 1) large males that construct nests and care for eggs and wrigglers; 2) medium-sized males that mimic female coloration and behavior and that will join a spawning pair to release sperm; and 3) small sneaker males that hang out near nests hidden by vegetation or rocks will dash in to a spawning pair, release sperm, and quickly hide again. The latter two types of males provide no parental care and essentially parasitize the parental care of the large males.
Once male parental care is present, it is thought that if predation pressures become sufficient that the male alone cannot successfully raise the brood, then biparental care will evolve. There are some noteworthy examples of biparental care in diverse groups of fishes. Biparental has only been reported in one coral-reef species, a damselfish Acanthochromis polyacanthus (family Pomacentridae). In this species, both parents will guard the eggs, wrigglers, and free-swimming fry. Many bullhead catfishes (family Ictaluridae) are also biparental. For example, the black bullhead catfish Ameiurus melas will dig a tunnel into the floor of a lake, and the male and female go into the tunnel together to lay and care for eggs. After the young become free-swimming, the parents and offspring exit the tunnel, and both parents care for the young.
So, how do cichlids fit into the picture? It is likely that parental care in cichlids evolved from this basic substrate guarding of eggs and nest, and has taken on some amazing new forms. Interestingly, there are no substrate spawning cichlids with male-only care. It is likely that the high predation pressures experienced by most cichlids strongly selects for biparental care.
Almost all biparental fishes are monogamous, but there are different forms of monogamy. Monogamy may consist of a pair staying together for a single spawning or for multiple spawnings. Many aquarists often find the same pair breeding with each other for several spawnings, often termed a pair bond. The typical biparental cichlid is sequentially monogamous, meaning that a male and female will pair for a spawning, and for subsequent spawnings they may mate with the same partner or find a new one. The question of what determines when an individual will stay with a current partner or find a new one has not been resolved. There are numerous cichlids that are sequentially monogamous and biparental, one of which is a cichlid we all know and love, the convict cichlid Cryptoheros (Archocentrus) nigrofasciatus. The extent to which this occurs in the wild remains to be shown.
In biparental cichlids, a male and female will court and eventually pair. The pair will then search for a suitable spawning habitat (a flower pot in aquaria; in the wild, a cave formed by stacked rocks or tree roots). The pair will guard the eggs, wrigglers, and fry. The female typically fans the eggs and the male guards the site from intruders, which are often other cichlids looking for food, or ubiquitous predators such as tetras. When the eggs hatch, the female will take any straggler eggs into her mouth and break the egg case so the offspring hatches at the same time as its brothers and sisters. The hatchlings will be moved (by mouth) to a pit the parents dug before the eggs were laid. While the hatchlings are in these pits the female will stay close by guarding them, and the male guards the surrounding area. Periodically the pair will move the wrigglers to a different pit. Once the offspring start swimming the parents actively defend the swarm as it moves slowly along the bottom of the tank or river. When a predator comes too close to the family the female will flick her pelvic fins as a signal for the offspring to “hit the deck”—go to the substrate and not move. Parents will also actively feed the offspring by pushing their bodies against the substrate and quickly moving their fins to stir up the sand and release microbes and algae for eating. A parent, typically the female, may also grab the edge of a leaf with her mouth and turn it over to expose the food morsels on the other side. Eventually the offspring will disperse. There does not appear to be a set age or size at which the offspring leave their parents.
Some cichlids take feeding the offspring to an extreme. For example, in many large Central American cichlids, the offspring eat nutritious mucous from the bodies of the parents. The parents produce this mucous specifically for the fry to feed on, and it even contains growth hormone. In the most extreme case, in wild discus, genus Symphysodon, the fry will not survive without eating parental mucous.
There are also some interesting species that do things slightly differently. In the wolf cichlid Parachromis dovii, brightly colored males found in river habitats do not participate in parental care, while brightly colored males in the lakes of Nicaragua are polygamous. Such a male has several females in a territory and sequentially makes his rounds helping each female care for the offspring for part of the time. An interesting question in the wolf cichlid species is whether the differences observed in the two populations are due to genetic differences in the populations, or if, given similar environmental conditions, each population could exhibit both behaviors.
Another interesting cichlid is the West African kribensis Pelvicachromis pulcher. The males compete with each other and hold territories, while females have bright purple bellies and also actively complete with each other for males; then the pair together will raise the offspring.
Substrate spawning with biparental care is widely considered to be the ancestral state in cichlids. Mouthbrooding has evolved several times in cichlids, with biparental mouthbrooding evolving first, then uniparental mouthbrooding. An interesting split in the family in terms of mating system is that 95 percent of the mouthbrooding genera occur in Africa, and 70 percent of the substrate-guarding genera occur in the New World. It still remains to be seen exactly what this geographic difference reflects.
One of the most incredible reproductive strategies that exists is delayed sequential biparental mouthbrooding. The Geophagus sp. “red head Tapajos” cichlid from Brazil is one such species. In this system, the pair lays eggs on a hard substrate and guards them, and when the wrigglers hatch one parent will pick them up and retain them in its mouth for a period of time. Then the offspring will be transferred to the other parent. This system has puzzled researchers and cichlid enthusiasts because it is so weird, namely, the parents are paying the costs of substrate spawning (eggs exposed to the environment) as well as the costs of mouthbrooding (not being able to eat for a period of time).
There are also some incredible biparental immediate mouthbrooding cichlids. An interesting species is the zooplanktivorous cichlid, Microdontochromis sp., found in Lake Tanganyika, which will sequentially swap who is mouthbrooding the offspring. This species is found in the open water and will circle and spawn in the middle of the water column. The female picks up the eggs as they spawn (before they fall to the bottom of the lake), then after a certain amount of time she will transfer the offspring to the male.
While mouthbrooding is almost the norm in East African cichlids, it is not limited to cichlids. For example, two species of bagrid catfish found in Lake Tanganyika, Phyllonemus filinemus and Phyllonemus typus, are also biparental mouthbrooders. Unlike cichlids, these catfish are nocturnal so there is far less known about their behavior than of diurnal cichlids. The male or the female will solely incubate the offspring until they reach a certain size, and then the pair will mouthbrood or guard.
A particularly interesting aspect of the evolution of mouthbrooding in cichlids is the close association it has with the evolution of female-only care. In fact there are only two species with male-only mouthbrooding in cichlid fish, both in the Sarotherodon genus. However, in the labyrinth fishes, family Osphronemidae, genus Betta (e.g., Siamese fighting fish), approximately 70 percent of the total species exhibit male-only mouthbrooding. A male will take eggs into his mouth and incubate them for up to four weeks. Unlike cichlids, where the one instance of paternal mouthbrooding is thought to have evolved from biparental mouthbrooders, paternal mouthbrooding in bettas is thought to have evolved from bubblenesting male care.
For female-only mouthbrooding in cichlids, the theory is that the typical division of parental behaviors between the sexes (i.e., females doing more of the fry-directed behavior and males doing more of the territorial behavior) may have predisposed a female to retaining the offspring in her mouth, creating an opportunity for the male to desert without adversely affecting the offspring’s survival. Males also benefit from deserting in that they can seek out new mates and potentially sire more offspring. In cichlids, female-only mouthbrooding has led to the mating systems in which an individual male will mate with several females and an individual female will mate with a single male for a spawning (called polygyny). In these species we often see exaggerated male features used to attract females, including bright coloration, bower building, and territoriality.
One mating system, known as a lek, consists of many males who all have nests or bowers near each other and females will come in as a group and examine the males. The males will display heavily and a female will mate with the male she likes the most. The pair will begin by circling each other, and when a female lays an egg she will turn and immediately pick it up. Often a male will have egg spots on his anal fin, and periodically during mating he will display this fin on the nest floor. The female will peck at the spot on the fin. It is thought that males ensure fertilization by releasing sperm when a female pecks at the anal fin. An example of a species with this mating system is Astatotilapia calliptera.
There are also species in which males have harems. This is when each male has a territory with several females in it and he mates with all of them. One interesting example of this system is the shell-dwelling cichlids of the genus Neolamprologus. A male defends the territory while the females provide most of the offspring-directed care. Females with their offspring live in shells during the brood cycle, and a male will have several shells in his territory. Males even steal each other’s shells and evict females and offspring from them. This is because good, large shells are a more limited resource than the females themselves.
Within maternal mouthbrooding there are two strategies commonly seen. There are species that incubate the eggs and then release the offspring once, after which the female will not take the offspring back into her mouth; this is known as semelcavous mouthbrooding. Species that exhibit this strategy include Stomatepia pindu, a West African Crater Lake cichlid. Other species will take offspring back into the mouth if a dangerous predator appears after the initial release; this is known as iterocavous mouthbrooding. Examples of this strategy include the South American Geophagus steindachneri and the African Pseudocrenilabrus multicolor. Both are very interesting species that will go around and suck up offspring (like a vacuum) when a predator comes near, or signal the offspring with a pelvic fin flick and head titled down, open mouth posture, to swarm and swim into her mouth. Offspring will also swim up to the female’s mouth and try to get in if they sense danger.
The evolution of parental care strategies in externally fertilizing fishes is thought to start with no care, then evolve to male-only care, then biparental care, and finally female-only care. Examination of the cichlids supports this direction of evolution. There are numerous mating strategies associated with these different care traits. In general, biparental care is associated with monogamy and uniparental care (both male-only and female-only) is associated with polygyny (one male spawns with many females) and promiscuity. But, as with everything in natural world, it is variable, and notable exceptions arise.