Mysterious mouthbrooders

(This article was originally published in Cichlid News Magazine, Jan-99 pp. 32-33, It is reproduced here with the permission of author Ron Coleman and Aquatic promotions).

Mouthbrooding is so common in cichlids that many aquarists may not realize that it is a rare and specialized form of parental care. Mouth-brooding has evolved at least eight different times in fishes in such diverse groups as arowanas, silurid catfishes, cardinalfishes, jawfishes, and anabantoids (Oppenheimer, 1970), but the habit has reached its zenith in cichlids, where the behavior has developed independently in South American, West African, and African rift lake subgroups.

Oreochormis aureus female holding eggs. Photo by Juan Miguel Artigas Azas.

At first glance, the question of why a parent should mouthbrood seems relatively simple. Mouthbrooding provides the offspring with a great deal of protection. Also, the churning action by mouthbrooders is vital for embryo survival. In a classic example of good experimentation, Evelyn Shaw and Lester Aronson (1954) showed that the eggs of Tilapia macrocephala could not survive unaided outside the mother's mouth, and that the fungus that appears on dying eggs is not the killing agent but merely a secondary infection. Most impressive was an experiment in which they created large flows of water over the eggs, but by placing them in a special tube with slight depressions, did not allow them to "roll over." The sides of the eggs exposed to the current lived while parts of the eggs away from the flow died. This clearly demonstrated that the function of churning is to rotate the eggs so that all parts are exposed to oxygenated water.

But mouthbrooding is not without its costs, and the fact that it occurs inside the mouth means that much of the process remains mysterious. New techniques, carefully designed experiments, and diligent observation are revealing some of those mysteries. Using measurements of oxygen consumption, Mrowka and Schierwater (1988) found that female Egyptian mouthbrooders (Pseudocrenilabrus multicolor) do not have to eat more while mouthbrooding, but they likely use up substantial resources that they have to build up prior to the brooding period. To get a clearer picture of the costs, Smith and Wooton (1994) performed a careful manipulative experiment using a Lake Victorian mouthbrooder, Haplochromis sp. "argens". They set up two groups. As each female bred, it was assigned to either a "parental" or "nonparental" group. All females were weighed, and females in the nonparental group had their eggs gently removed. Sixteen days later, at the end of the normal oral incubation period, the fish were weighed again and any remaining young removed. The experimenters then monitored the time it took before each female spawned a second time. Females that mouthbrooded during the experiment showed significantly lower growth rates and took longer to spawn again, though they were partially able to make up for the loss of growth by feeding heavily between the period of parental care and the next spawning.

Sigal Balshine-Earn (1995) examined a similar question in the biparental mouthbrooder, Sarotherodon galilaeus. She too found that providing care had costs for females. Mouthbrooding increased the time to next spawning, reduced the number of eggs in subsequent broods, and cost the female in body weight. Males that mouthbrooded also suffered by losing weight and taking longer to spawn again.

Some mouthbooders can reduce the costs of parental care by feeding. A number of Tanganyikan mouthbrooders feed while incubating. Some species like Cyphotilapia frontosa and Tropheus duboisi feed both for themselves and to nourish their young, while others, such as Tropheus moorii feed only for the nourishment of the young (Yanagisawa and Ochi, 1991). Yasunobu Yanagisawa and his coworkers (1996) recently described intrabuccal feeding of the young in an undescribed species of Microdontochromis from the southern end of Lake Tanganyika. Unlike Cyphotilapia or Tropheus which graze algae or pick invertebrates and have large eggs, this fish has a few small eggs and eats tiny zooplankton in midwater. The young in the mouth also eat these copepods, so much so that they grow to fill the female's mouth. Then a most remarkable thing happens. The fry appear to switch from the female's mouth to a larger male's mouth. This is incredibly peculiar, because this fish lives in large schools, and it is hard to imagine how a female finds the father of her young. Why is this an important question'? Simply because an unrelated male is better off swallowing the young than incubating them!

The biggest cost to a mouthbrooder may be when something goes horribly wrong and it ends up mouthbrooding eggs or fry that don't belong to it. The parasitic behavior of the mochokid catfish, Synodontis multipunctatus, in Lake Tanganyika is the most famous example. The history of its discovery is rather interesting, because it was first reported by Pierre Brichard (1979) to hobbyists and only later confirmed by the scientific community (Sato, 1986). The first observations appear to be those of Mireille Brichard, Pierre's daughter, who wrote to him upon finding Synodontis fry in the mouths of Ophthalmotilapia nasuta females. At the time, the elder Brichard speculated that the catfish fry entered the mouthbrooder's mouth at night when she was lethargic. By 1983, the phenomenon had been observed by several aquarists; the true level of deceit was revealed by Lee Finley (1983) when he correctly speculated that the catfish spawn at just the right time and place to have their eggs picked up by the spawning mouthbrooding cichlid. Once inside the mouth, the catfish eggs develop more rapidly than the eggs of their unwilling host, hatch first, and then feed on the young of their host (Sato, 1986). The mouthbrooding parent appears oblivious to the ongoings and raises the catfish as if they were her own offspring. The behavior is so reliable that these catfish are becoming increasingly familiar to many hobbyists, because breeders can regularly spawn them in aquaria, using species like Astatotilapia calliptera (a Malawian mouthbrooder) that seem susceptible to being cuckolded, not having evolved any natural resistance to this sort of trickery.

Karen Kellogg and colleagues (1998) have added a new twist to the puzzle. They had previously documented that females in several species of Lake Malawi cichlids had multiple paternity in their broods (Kellogg et al., 1995), meaning that not all eggs were fertilized by the same father. Now, she has good evidence that in at least one species, Protomelas cf. spilopterus, not all the eggs necessarily have the same mother! This means that the brooding female is wasting her parental effort on unrelated fry. Using a molecular technique known as microsatellite analysis, Karen identified which of the fry in each of six broods belonged genetically to the mother that was mouthbrooding them. In four of six cases, broods contained foreign fry. How the foreign fry get in there, particularly at early developmental stages, is still a mystery. This species lives at the rock/sand interface in Lake Malawi and typically mates at low densities, i.e., females do not spawn in clusters as in some other cichlid species. Frenzied mass spawning could explain a female occasionally picking up a foreign egg, but that doesn't appear to be happening in this case. There are still plenty of mysteries to be revealed about mouth-brooders.

References

• Balshine-Earn, S. 1995. The costs of parental care in Galilee St. Peter's fish, Sarotherodon galilaeus, Animal Behavior S0:1-7.
• Brichard, Pierre, 1979, Unusual brooding behaviors in Lake Tanganyika cichlids. Buntbar. Bull. 74:10-12.
• Finley, Lee, 1983. Synodontis multipunctatus reproduction and maternal mouthbrooding cichlids - a cuckoo relationship? Buntbar. Bull. 98:17-18.
• Kellogg, K. A., J. A. Markert, J. R. Stauffer, Jr., and T. D. Kocher, 1995, Microsatellite variation demonstrates multiple paternity in lekking cichlids fishes from Lake Malawi, Africa. Proc. Roy. Soc. London 260:79-84.
• Kellogg, K. A., J. A. Markert, J. R. Stauffer, Jr., and T. D. Kocher, 1998, Intraspecific brood mixing and reduced polyandry in a maternal mouthbrooding cichlid. Behav. Ecol. 9:309-312.
• Mrowka, W., and B. Schierwater, 1988, Energy expenditure for mouthbrooding in a cichlid fish. Behav. Ecol. Sociobiol. 22:161-201. 164.
• Oppenheimer, J. R., 1970, Mouthbreeding in fishes. Anim. Behav. 18:493-503.
• Sato, T. 1986, A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323:58-59.
• Shaw, E. S., and L. R. Aronson, 1954. Oral incubation in Tilapia macrocephala. Bull. Amer. Mus. Nat. Hist. 103:378-415.
• Smith, C., and R. J. Wooton, 1994. The cost of parental care in Haplochromis "argens" (Cichlidae). Environ. Biol. Fishes 40:99-104.
• Yanagisawa, Y. and H. Ochi, 1991. Food intake by mouthbrooding females of Cyphotilapia frontosa (Cichlidae) to feed both themselves and their young. Environ. Biol. Fishes 30:353-358.
• Yanagisawa, Y., H. Ochi and A. Rossiter, 1996.Intra-buccal feeding of young in an undescribed Tanganyikan cichlid, Microdontochromis sp. Environ. Biol. Fishes 47:191.
• Oppenheimer, J. R., 1970, Mouthbreeding in fishes. Anim. Behav. 18:493-503.
• Sato, T. 1986, A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323:58-59.