Pseudocrenilabrus The Dwarf African Mouthbrooders: Part One: The Pseudocrenilabrus multicolor Complex

(This article was originally published in Freshwater and Marine Aquarium Magazine, Jan 1982; pp. 30-35, 59-63. It is here reproduced with the permission of author Dr. Paul V. Loiselle).

In 1903, the German aquarist Schoeller reported upon his experiences with a small cichlid from Egypt. The fish he described as is today known as Pseudocrenilabrus multicolor, and his extremely detailed article, which could well serve as a model for contemporary writers on aquaristic subjects, represents the first published account of a haplochromine as an aquarium fish. Schoeller's fish, under the vernacular name of Egyptian Mouthbrooder, has been available to aquarists ever since. Indeed, until relatively recently, it was the only representative of this largest and most diverse of cichlid lineages available in the hobby. Time has changed this state of affairs. Nevertheless, it is fitting that, at a time when the aquarist is literally inundated with larger, more spectacular haplochromines from the Great Lakes of Africa, due consideration be given to their precursors, the smaller but equally desirable species of the genus Pseudocrenilabrus.

Until very recently, the species of this genus were placed in the genera Haplochromis or Hemihaplochromis. While contemporary ichthyologists accept the conclusion of Wickler (1963) that these cichlids are generically distinct from Haplochromis, they are barred by the provisions of the International Code of Zoological Nomenclature from utilizing the name he proposed for this assemblage of haplochromines. Trewavas (1973) has established the synonymy of the genera Pseudocrenilabrus Fowler 1934 and Hemihaplochromis Wickler 1963, and under the Rule of Priority, the older published name is the scientifically correct one for the genus. Though some recent reference works (Goldstein, 1973; Mayland, 1978; Staeck, 1975, 1977) have incorporated the new nomenclature in their treatment of these cichlids, for many readers this essay will be in large measure a review of some familiar fishes sporting an unfamiliar generic name. For the benefit of those aquarists inclined to fume about "arbitrary" changes in the scientific names of fishes, I will attempt to present the history of the events leading up to the present situation. This will, hopefully, provide a useful example of how such taxonomic problems arise and are resolved.

In 1934, the late Henry W. Fowler published a report on a series of marine and fresh-water fishes from Natal and Zululand in South Africa. In this paper, he described a new genus of wrasse, Pseudocrenilabrus, based upon a single specimen. Here matters rested until 1963, when Dr. James Boehlke of the Philadelphia Academy of Science informed Dr. Ethelwyn Trewavas, then on a visit to the United States, that he believed the holotype of this wrasse to be a cichlid. His suspicions were confirmed when Trewavas examined the entity in question and found it to be a specimen of the fish originally described by the German ichthyologist Weber in 1897 as Chromis philander and widely referred to in the subsequent literature as Haplochromis philander. In charity let us assume that in this instance Fowler was aided in his confusion of the Families Cichlidae and Labridae by a faulty locality label!

The same year that saw Trewavas' discovery of the true nature of Pseudocrenilabrus also saw the publication of a most important paper by the German ethologist Wolfgang Wickler, in which behavioral characteristics were, for the first time, utilized as the principle element in the definition of a cichlid genus. Dr. Wickler found that the Egyptian Mouthbrooder of aquarists, Haplochromis multicolor, differed from the two other Haplochromis studied by him in details of the male color pattern and in some important aspects of its reproductive behavior. Unlike other Haplochromis species, males of the Egyptian Mouthbrooder were found to lack orange or yellow pseudo-ocelli on their anal fins, possessing instead an orange-red distal spot at the tip of the anal fin. Wickler further reported that in H. multicolor fertilization of the ova by the male began almost immediately after oviposition, contrary to what was observed in the other Haplochromis species studied. He consequently established a new genus, Hemihaplochromis, for the Egyptian Mouthbrooder and by extension, for any other haplochromine species displaying a comparable color strategy. On the basis of shared elements in their color pattern, Jubb (1967) placed Haplochromis philander in Hemihaplochromis. By 1970, the nomen Hemihaplochromis had generally been accepted by ichthyologists, ethologists and aquarists alike.

Enter the Rule of Priority. The International Code of Zoological Nomenclature, article 23, states: "The valid name of a taxon is the oldest available name applied to it, provided that name is not invalidated by any provision of this Code or has not been suppressed by the Commission." The only exceptions to this rule, established to provide a stable criterion for the determination of the validity of the scientific names of animals, are (a) names that have been expressly validated by the Commission, an action seldom taken, or (b) names that have gone unused as senior synonyms in the primary zoological literature for more than fifty years. These latter are referred to as nomina oblita, literally "forgotten names." It may be argued that the name Pseudocrenilabrus, describing a wrasse, is not appropriate for a cichlid. The Rules are adamant on this point too. Article 18(a) states: "A genus- or species-group name, once established, cannot afterwards be rejected, even by its own author, because of inappropriateness." Consequently, however little ichthyologists or aquarists may like the fact, Pseudocrenilabrus, as indicated by Trewavas, is without doubt the correct generic name for the cichlids formerly referred to in the scientific literature as Hemihaplochromis.

Setting taxonomic protocol aside, we can define the genus Pseudocrenilabrus as comprising small cichlids with the upper pharyngeal apophysis of the Haplochromis type and a moderately protractile upper jaw [see Fryer and Iles (1972) for a discussion of the two means by which cichlids articulate the upper pharyngeal bones to the base of the skull.] The teeth present in the outer row in the jaws are unequally biscuspid anteriorly, biscuspid or conical posterolaterally, while those of the inner rows are tricuspid. The arrowhead-shaped lower pharyngeal bone is slender and covered with delicate, unequally bicuspid teeth. The scales are ctenoid. The lateral line is present as a series of simple pores and is frequently interrupted. The caudal fin is rounded, a feature that distinguishes this genus from all other haplochromines. The bases of the unpaired fins are unscaled. A metallic golden or coppery zone is present in the shoulder region in males of all species and in females of several. Males lack pseudo-ocelli on their anal fins. Instead, they possess a distinct red or orange spot on the distal tip of the anal at some time during their lives. In most cases, this marking is retained throughout life. All are maternal mouthbrooders characterized by possible partial extrabuccal fertilization of the eggs by the male and direct mouthing of the male's vent during the spawning act by the female.

The genus comprises three nominal species, though its actual taxonomic situation is considerably more complex than this would, on the surface, suggest. One species, Pseudocrenilabrus philander, comprises a complex of distinctive, geographically separate populations, all enjoying some degree of reproductive isolation. Another, P. multicolor, consists of two highly distinctive, quite possibly specifically distinct populations. Whether such populations are best treated as species, subspecies or simply left without formal taxonomic designation is a question only further research can satisfactorily resolve. But, as several of them have been introduced as aquarium fish, aquarists must confront a highly plastic and potentially confusing situation. Killifish fanciers have learned to live with comparable situations as a matter of course and I think that cichlid enthusiasts working with Pseudocrenilabrus would do well to borrow a few points of procedure from them.

First of all, color forms should be referred to by their locality of origin whenever this is known, i.e., P. philander / Natal, P. philander / Lake Chilwa, P. multicolorl / Uganda. This approach provides a convenient handle for the discussion and dissemination of these cichlids pending formal clarification of their status. Secondly, every possible effort must be made to maintain aquarium strains of these fish uncontaminated by hybridization with other forms of the same nominal species. As has been done with killifish, such hybridization should be carried out strictly as a tool to ascertain the relationships between these forms. It should be undertaken only under controlled conditions and any hybrids produced should be destroyed once they have served their purpose. Under no circumstances should hybrids of any cichlids be released for sale or trade. Their presence in commercial channels can only obscure what is, in many cases, an already turbid taxonomic situation while posing the substantial risk of contamination of parental gene pools through inadvertent back-crossing. Scientifically minded aquarists can contribute much to the study of Pseudocrenilabrus systematics, but careless or indifferent hobbyists can cause the loss of distinctive phenotypes of these nominal species through such random hybridization and release into commercial channels of hybrid fry. The best way to guarantee against accidental hybridization in captivity is to always house different forms of the same nominal species separately.

All of the forms comprised within the three nominal species of the genus share a number of attributes in common, which dictate a common maintenance strategy in captivity. All will take any of the usual live or prepared foods so long as they are offered in an easily swallowed form. None will prey upon any fish too small to be easily swallowed, though as we shall see, the belligerence of sexually active males imposes other constraints upon the selection of tank-mates for these cichlids. These small haplochromines are not given to gratuitous destruction of rooted plants. Digging is restricted to males and occurs only in the context of reproduction. All will prosper over a wide range of pH and hardness values. To a substantially greater extent than that seen in other extra-lacustrine haplochromine species, Pseudocrenilabrus are intolerant of the pollution of their environment by dissolved nitrogenous wastes. Excessive crowding and indifferent tank maintenance are the chief causes of fry mortality. Chronically high nitrite levels, though rarely killing them outright, lower the resistance of adults to systemic bacterial infections that invariably do prove fatal. The ease with which Pseudocrenilabrus adapt to a wide spectrum of local water conditions suggests that regular partial water changes are the simplest means of satisfactorily managing the nitrogen cycle in their aquaria. When proper attention is given to this aspect of their maintenance, Pseudocrenitabrus are no more difficult to maintain than are their distant relatives, the riverine Haplochromis (Loiselle, 1978).

Though these are small cichlids, rarely exceeding 10.0 cm SL in nature, sexually active males display a level of aggressiveness quite out of proportion to their size. A male 4.0 cm SL is easily capable of totally monopolizing an area 60 cm square, to the extreme discomfiture of any fish daring to venture into the lower half of the water column. In practical terms, this translates into one male/80 1 aquarium at any stocking density under a single fish/liter of tank volume. At lower densities, a linear dominance hierarchy will emerge among males, with the dominant fish eventually liquidating those beneath him in the peck order. Yet this belligerence cannot entirely cancel out the fact that these fish, while falling outside of my definition of a dwarf cichlid on behavioral grounds (Loiselle, 1979, 1980), do fall into the dwarf category with regard to size. Taken with the apparent inability of males to exercise any discernible degree of discretion in their choice of targets, this sharply limits the selection of possible tank-mates for any Pseudocrenilabrus species.

Many aquarists make the error of trying to keep Pseudocrenilabrus in the company of Haplochromis species or even of mbuna. The consequences are invariably disastrous. Both sexes of the smaller Pseudocrenilabrus tend to be out-competed at feeding, while females come in for a great deal of general harassment at all times. Efforts by males to hold a territory bring them into conflict with Haplochromis males that are both absolutely larger and whose jaws are disproportionately bigger in the bargain. Those males Pseudocrenilabrus that are not seriously injured in outright conflicts lose condition in the face of continued aggression by their larger relatives, eventually to fall prey to stress induced systematic bacterial infections. Given that their habitat preferences rarely bring them into association with sympatrically occurring Haplochromis species in nature, such an outcome is not surprising. Yet, when the sorry progress has run its full course, the culpable aquarist typically blames the Pseudocrenilabrus for lack of hardiness, condemns the genus to perdition, and resolves to steer clear of its species in the future. In reality, his unfortunate experiences are the fault of his own ignorance of the behavioral limitations of these cichlids and could have been easily prevented.

Pseudocrenilabrus also do poorly when housed with either Neotropical or African substratum-spawning cichlids. Such tank-mates grow progressively less inclined to put up with the aggressiveness of male Pseudocrenilabrus as they, themselves, come into breeding condition. The automatic two to one odds their mating system brings to such encounters augur poorly for the long term prospects of any haplochromine under such conditions, as I have pointed out previously (Loiselle, 1978). Pseudocrenilabrus are best kept in small groups comprising a single male and three to five females. If space requirements dictate that they be housed with other cichlids, members of the genus Sarotherodon make the best companions. They are too large to run any danger from the attacks of even the most bellicose male Pseudocrenilabrus and rarely deign to retaliate even under persistent harassment. Like other haplochromines, males of these cichlids will, when sexually active, attack non-cichlids that habitually move about near the bottom. They tend to ignore fish that usually swim in midwater or near the surface provided such companions are too large to make a convenient mouthful. The larger barbs and Australian rainbowfishes make excellent dither for Pseudocrenilabrus.

Pseudocrenilabrus multicolor was described by the German aquarist Schoeller in 1903, making it the doyen of all the haplochromine species available to hobbyists as well as one of the very first cichlid species to be spawned in captivity. Schoeller's fish were collected from Lake Mareotis in Northern Egypt. The ichthyologist George A. Boulenger, then working at the British Museum, considered (1907) Schoeller's fish to be synonymous with a fish from a coastwards flowing stream in East Africa described in 1893 by a German colleague, Pfeffer, under the name Ctenochromis strigigena. He attributed Schoeller's material, as well as several lots of fishes from the Upper Nile in the Sudan and from the Lake Victoria basin to that species. Boulenger thus used the nomen Haplochromis strigigena for the Egyptian Mouthbrooder in his monumental Catalogue (1915).

In 1922, his successor, C. Tate Regan, found that the type material of Haplochromis strigigena was actually referable to another, previously described species, Haplochromis bloyeti (Sauvage 1883) and that, contrary to Boulenger's conclusion, the material from the Nile and Lake Victoria basins ascribed to H. strigigena was indeed representative of a different species. Following the Rule of Priority, whose operation we have already considered, he therefore resurrected Haplochromis multicolor as the oldest available name for these cichlids. At least with regard to their specific name, the scientific literature has followed Regan to the present day, but as is so frequently the case, the aquarium literature did not. Aquarists have thus been faced with reference works either listing Haplochromis strigigena as the scientific name of the fish called the Egyptian Mouthbrooder under the well-intentioned but mistaken belief, probably garnered from perusal of Boulenger's Catalogue, that as the earlier of two published nomina it has priority over H. multicolor. Alternatively, the Egyptian Mouthbrooder has been discussed twice in the same work, once under each name! As indicated previously, this is the species studied by Wickler, who made it the type species of his genus Hemihaplochromis.

The Egyptian Mouthbrooder has been a staple of the aquarium hobby ever since its introduction by Schoeller. Until quite recently it was believed that the Ugandan populations of P. multicolor were identical to those native to Egypt and the Sudan. In the spring of 1972, Ugandan fish were imported into the United States in quantity. They had been brought in sporadically somewhat earlier by German importers and distributed under the trade names "Haplochromis kiravira" or "Haplochromis kirawira." As reference to the accompanying illustrations will indicate, the Ugandan fish differ markedly in color pattern from the Egyptian fish previously available to aquarists.

It would appear that Pseudocrenilabrus multicolor is polytypic, with two distinct populations. The first occurs in the Nile, inhabiting that river in Egypt as well as its tributary streams in the Sudan, including the Bahr-el-Jebel. The naturalist Loat's account of the Sudanian populations of P. multicolor as reported by Boulenger (1907) leave no doubt of their identity with Schoeller's fish. Very likely the Lake Albert populations of P. multicolor should be grouped with this predominantly riverine assemblage of populations. Lake Albert and the Nile are fully connected and the ichthyofaunas of both are virtually identical. Interestingly enough, there is no record of P. multicolor from Lake Turkana, formerly known as Lake Rudolph, but its presence there would not be surprising. Given the close correspondence between the fish faunas of the Nile River and Lake Turkana, one would expect P. multicolor to be represented there by the Nile population. The second of these two distinctive populations appears restricted to the basin of Lakes Victoria and Kyoga, separated from the lower Nile basin by Murchison Falls, to the basins of Lakes George and Edward, which are cut off from Lake Albert and the lower reaches of the Nile by the Semliki Rapids, and to many minor lakes in northwestern Uganda and northeastern Rwanda.

The status of these distinctive populations remains to be determined. For the present, I would suggest retaining the traditional Egyptian Mouthbrooder as a designation for the Nilotic populations and utilizing the designation of Ugandan Mouthbrooder for those occurring south of Murchison Falls and the Semliki Rapids. The latter have been available through commercial channels under the trade names given earlier, as well as under the very misleading name of Haplochromis fasciatus, which is properly that of a morphologically distinctive haplochromine native to the lower reaches of the Congo River, many thousands of miles to the west of Uganda. In several recent German publications (Mayland, 1978; Richter, 1980) this fish has also been discussed under the name Pseudocrenilabrus philander dispersus, a very different congener native to southern Africa that will be discussed in the second portion of this article.

Both forms of P. multicolor are in the hobby at present, though the Ugandan Mouthbrooder tends to be of sporadic and often very localized availability. Interestingly, there tends to be a great preponderance of males among imported Ugandan fish. As is typically the case with haplochromines, the males are by far the more colorful sex. The unbalanced sex ratios of imported Ugandan Mouthbrooders may reflect either ignorance of the true appearance of the female or alternatively, a reluctance to ship dull colored specimens that may not sell well. Such a state of affairs is not unfamiliar to hobbyists who work with the endemic haplochromines of Lake Malawi. Whatever its cause, it greatly hinders efforts to establish tank-reared populations of these cichlids, a fact which in my more cynical moments offers itself as another plausible explanation for the occurrence of such imbalances.

Very little is known of the ecology of the Egyptian populations of P. multicolor. The Lake Victoria populations of the Ugandan Mouthbrooder have, on the contrary, been studied by Welcomme (1969, 1973). He found this species a characteristic inhabitant of the fringing waters of larger rivers, of small streams and of swamps along the margins of both rivers and lakes. While occurring in the estuaries of small streams flowing into Lake Victoria, P. multicolorl Uganda is not typically found in the lake itself. As we shall see, this avoidance of true lacustrine habitats parallels the distribution pattern of P. philander in the Lake Malawi basin. Presumably competitive pressure from larger Haplochromis operates to prevent effective colonization of such habitats by Pseudocrenilabrus species. In this context, it would be interesting to know more of the ecology of P. multicolor/Uganda in the small lakes in Uganda and Rwanda that lack extensive assemblages of endemic Haplochromis species.

Within its chosen habitat, P. multicolor / Uganda occurs over a wide range of substrata, ranging from sand and clay through mud with a very high content of organic matter. While emergent and floating aquatic plants are abundant in such habitats, submerged plants are not. Blooms of green and blue-green algae are not uncommon, and the stems and leaves of aquatic plants generally support a rich diatom flora. The Ugandan Mouthbrooder forages for its food over the bottom and among the leaves and stems of aquatic plants. Aquatic insect larvae appear to be staple items, but quantities of diatoms are also eaten. This may explain the intense golden yellow coloration seen in freshly imported specimens of P. multicolor / Uganda. Such coloration certainly seems to be strongly influenced by diet, for specimens I captured for photographic purposes during a visit to Jinja, Uganda in the spring of 1971 faded markedly within 24 hours of being placed in a holding tank.

The spawning behavior of Pseudocrenilabrus multicolor from Egypt. The male actively displays to passing females from a previously excavated pit (1). A ripe female eventually responds to his displays by following him into its confines (2). The pair then begins a period of reciprocal circling (3-5), which is accompanied by mutual vent nudging. The gentle butting of the female's vent by the male (6) seems to trigger oviposition. The female picks up the eggs immediately (7), then turns to follow the male (8 & 9). As she does so, she nudges his vent (10). Fertilization appears to occur at this point. Note that her mouth is oriented towards the male's vent, not towards the orange-red spot on the tip of his anal fin (11). This sequence is repeated (12-15) until the bulging jaw of the female (16) indicates that she is spent.

The Egyptian Mouthbrooder can tolerate temperatures as low as 13° C for short periods of time, while prolonged exposure to 16° C appears to do it no harm. Since this cichlid ranges as far north as the Nile Delta, this is hardly surprising. Data are lacking on tolerable minimum temperatures for the Ugandan Mouthbrooder. Given its exclusively tropical distribution, it seems imprudent to expect a tolerance for temperatures lower than 18° C. Both populations of P. multicolor can tolerate briefly temperatures as high as 32° C, but a range of 24° -29° C is more appropriate for their aquarium maintenance. Like other haplochromines, all Pseudocrenilabrus eat more heavily, behave more aggressively and have a shorter developmental interval at the upper end of their preferred temperature range.

Like all their congeners, both populations of this species are tolerant of a wide range of water conditions. In nature, they typically occur in moderately hard, slightly alkaline water, but as long as he avoids extremes of either pH or hardness, the aquarist need not concern himself greatly about these aspects of water chemistry. Stress induced by build-up of nitrogen cycle by-products is a more serious problem. The Ugandan Mouthbrooder is particularly sensitive to such pollution and must have good tank maintenance and a program of regular partial water changes if it is to prosper in captivity. Both forms devour with gusto any of the usually available live and prepared foods. The golden yellow and red coloration of these cichlids is very sensitive to dietary influences. To maintain it at its fullest, the prudent aquarist will offer his specimens a diet rich in the appropriate precursor substances. The easiest way to get such supplements into these distinctly carnivorous little cichlids is to use one of the commercially available color enhancing foods.

Nothing is known of the reproductive ecology of the Egyptian Mouthbrooder. In nature, males of the Ugandan Mouthbrooder move into clear, plant-free waters about 30 cm deep to construct their nest pits. These tend to be clustered in areas having relatively little water movement and a firm but muddy bottom. Females visit these nesting areas only to spawn and leave them afterwards for nursery grounds in shallow water, generally 10 to 20 cm deep. At 25° C, females carry for fourteen days, at which point they move into very shallow water, five centimeters deep or less, and release the free-swimming fry among stems of submerged grass or other emergent vegetation. The female will continue to protect the fry for at least two days after their initial release. Interestingly enough, Welcomme indicates that this species follows a seasonal pattern of spawning, with reproductive activity limited to the rainy season.

Both the Egyptian and Ugandan Mouthbrooders spawn in the same manner in captivity. Males excavate simple depressions in the substratum from which they conduct their extremely vigorous courtship of any females in their immediate vicinity. As their attentions can sometimes grow dangerously overbearing, it is best to house these diminutive haplochromines on a harem basis and have plenty of cover available for females to fall back on until they are ready to spawn. A receptive female, whose abdomen is often extremely swollen, will follow a male to his depression, wherein both fish begin the reciprocal circling movements that eventually lead to spawning. Both extra- and intra-buccal fertilization of the eggs appears to occur. According to Wickler (1963), the red spot at the tip of the male's anal fin serves as an egg dummy in the Egyptian Mouthbrooder. My own observations do not confirm this conclusion, however. As the accompanying photos indicate, direct mouthing of the male's vent by the egg-laden female characterizes the reproductive act in this species.

The olive to beige, somewhat pyriform ova measure c. 2.5 mm along with their major axis. They can number from 6 to over 100, depending upon the size and condition of the female. The developmental interval for these fish is 10 days at 29° C. Ovigerous females are exemplary mothers and will carry to full term even in a community situation. However, if the objective is to save any fry, the hobbyist should move such females into a separate nursery tank, set up in the manner indicated for ovigerous female Haplochromis (Loiselle, 1978). The fry measure 6.5 mm-7.5 mm SL upon release. While the female will continue to protect her offspring for several days following their initial release, such efforts are invariably futile in a community setting and superfluous in the privacy of a nursery tank.

Welcomme (1973) reported that in nature, the number of free-swimming fry released by females of the Ugandan Mouthbrooder ranges from 17 for females in the 3.0 cm-3.5 cm size range to 63 for females in the 5.6 cm-6.0 cm range, a considerably smaller number than would be expected given the number of eggs typically spawned by females in these size classes. The same pattern is characteristic of the Egyptian Mouthbrooder in captivity. Welcomme ascribes the discrepancy to wastage generated by relatively inefficient mechanisms of fertilization and brooding. Insofar as partial cannibalism of her brood during incubation by an ovigerous female can be described as inefficient, I would concur with the latter hypothesis, but I consider it very unlikely that any eggs manage to escape fertilization given the combination of extra- and intra-buccal fertilization practiced by members of this genus.

The slender fry of both populations can take the smallest Artemia nauplii, micro-worms and finely powered prepared foods for their initial meal. They will not tolerate dirty or crowded tanks, but are otherwise easily reared. Growth is relatively slow. Welcomme reports that in nature, the Ugandan Mouthbrooder does not attain sexual maturity until the seventh month post-release, as 2.8 cm SL for males, 2.6 cm SL for females. In captivity, secondary sexual coloration becomes evident in males of both populations at c. 1.8 cm SL, a point in growth generally attained between the eighth and tenth week post-release. Sexual maturity is attained between fourteen and sixteen weeks post-release, at lengths of 2.5 cm SL and 2.0 cm SL for males and females respectively.

In summary, the Egyptian Mouthbrooder is probably the hardiest and most easily bred member of the entire genus Pseudocrenilabrus. The Ugandan Mouthbrooder is somewhat more demanding, given its sensitivity to tank fouling and susceptibility to stress-induced systemic bacterial diseases. Its brilliant coloration makes it well worth a little additional effort however. Hopefully tank-reared fish will prove somewhat hardier than their wild progenitors, for this lovely little cichlid deserves the same wide popularity among hobbyists that its Egyptian counterpart has always enjoyed.