Overlapping territory of the benthophagous cichlid fish, Lobochilotes labiatus, in Lake Tanganyika

Synopsis Feeding territories do not usually overlap in the same fish species. We studied overlapping territories and feeding behaviours of a benthophagous cichlid fish Lobochilotes labiatus Boulenger in a coastal area of Lake Tanganyika. Forty-four individuals of both sexes, 6–31 cm in total length, maintained territories in a 21 m × 25 m area. These could be regarded as feeding territories. The territories of similar-sized owners (usually different by less than 5 cm) did not overlap each other, but those of different-sized owners overlapped widely. Aggressive interactions were rarely observed between fish distinctly different in body size. Both large and small fish took benthic animals of the same kinds and of similar size. In contrast, the size of foraging sites (crevices) was different between them: the large fish foraged at large crevices and small fish at small crevices. This partitioning of foraging sites may enable the overlap of territories in this benthivore.     

Overlapping territories ofPseudosimochromis curvifrons males and other herbivorous cichlid fishes in Lake Tanganyika

Males of the herbivorous cichlid fishPseudosimochromis curvifrons established mating territories 3–10 m in diameter, which included both spawning and feeding sites. Territorial males attacked conspecific males and also other species. Only conspecific males were chased out of the territories. Territorial males attacked other species at the spawning sites while courting or waiting for females and at other sites in their territories while patrolling and foraging. Attacks against herbivorous species were more frequent than against non-herbivores since herbivores were much more abundant. Territories of four abundant herbivorous cichlids largely overlapped the territories ofP. curvifrons males. Symbiotic relationships were not detected between the species. Instead, they were aggressive towards each other but coexisted by segregating feeding sites in the overlapping areas. The aggressive coexistence ofP. curvifrons males with other herbivores may have resulted from the energetic costs of defending their relatively large territories against all food competitors. Interspecific food-resource partitioning may also have facilitated the coexistence.     

Depth-related differences in territory size and defense in the herbivorous cichlid,neolamprologus moorii, in lake tanganyika

Neolamprologus moorii, a small herbivorous cichlid of Lake Tanganyika, defends its territory against food competitors. Territory size and territorial defense were compared between two sites at different depths. In the shallow site, more fishes intruded into the territories than in the deep site, owing to the higher density fish population in the former. The territory holders in the shallow site attacked intruders more often, although the ratio of attacks to number of intruders was similar to that of the deep site. The territories in the deep site were larger and contained a greater amount of algae than the shallow site. The larger territory size in the deep site may have resulted from the lower cost of territory defense due to the lower competitor density and from the need to maintain a greater amount of food resources to compensate for lower algal productivity.     

Male foraging avoidance in female feeding territories in a harem polygynous cichlid in Lake Tanganyika

We studied foraging site partitioning between the sexes in Neolamprologus tetracanthus, a shrimp-eating Tanganyikan cichlid with harem-polygyny. Females maintained small territories against heterospecific food competitors within large territories of males, foraging exclusively at the inner side of their own territories (foraging areas). Males fed as frequently as females in their own territories, but mostly outside female foraging areas, although they frequently entered female territories and repelled food competitors from the territories. Soon after removal of the resident females, however, harem males, as well as many food competitors, invaded the vacant territories and intensively devoured prey of female foraging areas. This indicates that although female foraging areas appear to contain more food than outside the areas, harem males refrained from foraging there when the resident females were present. We suggest that harem males will attempt to keep female foraging areas in good condition, whereby they may get females to reside in male territories and/or promote female gonadal maturation.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

Evolutionary history of the endemic Lake Tanganyika cichlid fish Tylochromis polylepis: a recent intruder to a mature adaptive radiation

With an age of 9–12 million years (Myr) Lake Tanganyika holds the oldest and most complex species flock of cichlid fishes. It is believed to be of polyphyletic origin and rooted in nine ancient African lineages, six of which underwent diversification, while three remained monotypic. Here, the evolutionary history, route and timing of colonization were analyzed, as well as intraspecific genetic diversity of Tylochromis polylepis , the single albeit endemic representative of the tribe Tylochromini in Lake Tanganyika. The role of Tylochromis in the radiation was uncertain and the species was suggested to be either an ancient colonizer or a recent addition to the fauna. With 2.8–4.2% sequence divergence to four congeners living in Lakes Bangweulu and Mweru (Upper Congo River) as well as from Luozi River and Lake Etsotso (Lower Congo River), the species appears to be a recent colonizer, which is likely to have diverged from its riverine allies less than 510 000 years ago. The ability to enter an adaptive radiation at a highly mature stage with its densely packed species community and fine-tuned niche segregation seems remarkable. So far it was assumed that all Tanganyikan endemics evolved within the lake ecosystem by intralacustrine speciation, and that complex competitive interactions among endemics tighten the system against intruders. The intruding species can be classified as a generalist living over muddy bottom in the lake and in river estuaries. Microgeographic substructuring is suggested, possibly because of geographic segregation of breeding sites. Concerning the route of colonization, a downstream movement via one of the inflowing rivers situated in the south of Lake Tanganyika is suggested.     

Lunar synchronization of spawning in cichlid fishes of the tribe Lamprologini in Lake Tanganyika

Lunar synchronization of spawning was investigated for eight substrate brooding cichlid fishes belonging to the tribe Lamprologini. Their spawning activities all peaked during the second quarter of the lunar cycle. Comparison between their breeding styles and the degrees of spawning synchronization suggested that the nocturnal guarding-efficiency of eggs, especially exposed ones, is improved by the maximal amount of moonlight during full moon and, in species whose young leave the breeding sites about 2 weeks after spawning, the survival of dispersing young is enhanced by the darkness of moonless nights.     

Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish

We used nuclear and mitochondrial DNA (mtDNA) sequences from specimens collected throughout Lake Tanganyika to clarify the evolutionary relationship between Lamprologus callipterus and Neolamprologus fasciatus . The nuclear data support the reciprocal monophyly of these two shell-breeding lamprologine cichlids. However, mtDNA sequences show that (i) L. callipterus includes two divergent and geographically disjunct (North–South) mtDNA lineages; and that (ii) N. fasciatus individuals cluster in a lineage sister group to the northern lineage of L. callipterus . The two mtDNA lineages of L. callipterus diverged c . 684 kya to 1.2 Ma, coinciding with a major water level low stand in Lake Tanganyika, which divided the lake into isolated sub-lakes. This suggests that the two mtDNA lineages originated as the result of the separation of L. callipterus populations in different sub-basins. The incongruent phylogenetic position of N. fasciatus can best be explained by an ancient unidirectional introgression from L. callipterus into N. fasciatus. Remarkably, our data indicate that this event resulted in the complete mtDNA replacement in N. fasciatus . Our data suggest that hybridization occurred soon after the divergence of the two L. callipterus mtDNA lineages, probably still during the water level low stand, and that subsequently the invading mtDNA lineage spread throughout the lake.     

Monogamy in the maternally mouthbrooding Lake Tanganyika cichlid fish Tropheus moorii

Supported by evidence for assortative mating and polygynandry, sexual selection through mate choice was suggested as the main force driving the evolution of colour diversity of haplochromine cichlids in Lakes Malawi and Victoria. The phylogenetically closely related tribe Tropheini of Lake Tanganyika includes the genus Tropheus, which comprises over 100 colour variants currently classified into six morphologically similar, polyphyletic species. To assess the potential for sexual selection in this sexually monochromatic maternal mouthbrooder, we used microsatellite-based paternity inference to investigate the mating system of Tropheus moorii. In contrast to haplochromines in Lake Malawi, multiple paternity is rare or even absent in broods of T. moorii. Eighteen of the 19 analysed families were consistent with genetic monogamy, while either a mutation or more than one sire explained the genotype of one offspring in another brood. We discuss the differences in breeding behaviour between T. moorii and the Lake Malawi haplochromines, and evaluate additional factors or alternatives to sexual selection as promoters of colour diversification. A preliminary survey of other Tropheini species suggested that multiple paternity is infrequent in the entire tribe.     

Food habits and foraging behaviour of benthivorous cichlid fishes in Lake Tanganyika

Synopsis A study was made of the food habits and foraging behaviour of coexisting benthivorous cichlid fishes along the rocky northwestern coast of Lake Tanganyika. The five group-foraging species regularly found in the study area,Gnathochromis pfefferi, Lamprologus callipterus, Altolamprologus compressiceps, Lepidiolamprologus elongatus andLobochilotes labiatus, have different foraging techniques, although all eat shrimps (family Atyidae). Individuals of each species allow potential food-competitors to forage within its foraging area, increasing its own chances of finding shrimps disturbed by the foraging action of such competitors. In these five shrimp-eating species, group foraging thus occurs in a mutualistic context. A super-abundance of shrimps may allow the coexistence of shrimp-eaters with different foraging techniques, and furthermore, their coexistence itself may promote cooperative group-foraging among them. Three benthivorous cichlids,Neolamprologus mondabu, N. tretocephalus andN. leleupi, were indifferent to, or excluded, the group foraging species because these three individual-foraging species exploit different food items or employ similar foraging techniques to the group-foraging species.     

A field survey of the bredding habits of Eretmodus cyanostictus, a biparental mouthbrooding cichlid in Lake Tanganyika

Oral incubation of young or mouthbrooding reduces the selective advantages of care by two parents and thus biparental care is rare among mouthbrooding fish. We surveyed the breeding biology of Eretmodus cyanostictus, a biparental mouthbrooder from Lake Tanganyika, to understand what factors maintain biparental care. We found larger males than females, a male-biased sex ration and indications that spawning is synchronized around the full moon. These preliminary findings suggest that the benefits of desertion for males are low; males may maximize their reproductive success by helping raise young while females regain reproductive condition.     

Geometric morphometrics applied to viscerocranial bones in three populations of the Lake Tanganyika cichlid fish Tropheus moorii

Lake Tanganyika comprises the oldest and most diverse species flock of cichlid fishes. Many species are subdivided into numerous populations, often classified as geographical races, colour morphs or sister species. Unlike younger species flocks, in which speciation is accompanied by eco-morphological diversification that of Lake Tanganyika is at a mature stage with little further morphological change, most probably caused by stabilizing selection. This study addresses body shape differences among three genetically distinct but morphologically similar populations of Tropheus  moorii , by focusing on bony structures of the cichlid head. We test by means of geometric morphological methods whether shape changes in the cichlid head are based on particular osteological differences. Specimens were disarticulated enzymatically, and standardized digital images of the disarticulated bony elements were taken. A landmark system was established for the dentary, articular, premaxilla, quadrate and the preopercle. Only the dentary shows significant differentiation among the three populations. Since all three populations live in similar cobble habitats and occupy the same trophic niche, the observed difference in the shape of the dentary can either be explained by different directional selection due to subtle habitat differences, or by neutral drift constrained by borders enforced through stabilizing selection. Lack of difference might indicate stabilizing selection on bone shape.     

Resource control by territorial male cichlid fish in Lake Malawi

1. The rocky habitat communities of Lake Malawi contain a high diversity of ecologically similar, predominantly herbivorous, cichlid fish species. How so many species can coexist is still unknown.
2. Adult males of the majority of these species hold permanent territories which form dense multispecies mosaics across the shores.
3. The study examined six coexisting species of cichlids from the rocky habitat where males are known to control access to the algal food resources within their territorial space. These included four sibling species of the Pseudotropheus ( Tropheops ) species complex, which are specialized epilithic algal herbivores, and two sibling species of the trophically more generalist P . ( Maylandia ) species complex which feed upon both epilithic algae and plankton.
4. The hypotheses that both intraspecific and interspecific territoriality occur in these communities and that interspecific aggression initiated by territorial males is preferentially directed at species with the most similar diets to their own were tested.
5. It was found that males preferred to exclude conspecific intruders, while they tolerated intruders with different diets to their own. Also, male P . ( Tropheops ) preferentially excluded similar heterospecific dietary specialists, while male P. ( Maylandia ) tolerated similar heterospecific dietary generalists.
6. Based on this study, it is proposed that interspecific territoriality may be reducing competition between species with different diets and promoting their coexistence, while it may be enhancing competition between species with the same diet. Furthermore, it suggests that ecological generalism may be reducing the intensity of interspecific competition, while specializations for the same resources may be increasing competition.     

PERMANENT GENETIC RESOURCES: Isolation and characterization of microsatellite loci in the cichlid fish in Lake Victoria, Haplochromis chilotes

Twelve short tandem repeat markers were successfully isolated from a cichlid, Haplochromis chilotes, in Lake Victoria, and characterized in Haplochromis pyrrhocephalus. The microsatellite regions of these markers were found to have between two and 48 alleles with heterozygosity ranging from 0.07 to 0.97. No loci showed significant departures from the Hardy–Weinberg or linkage equilibrium after the Bonferroni correction (P > 0.05). Cross‐species amplification in other cichlids of Lake Victoria, Haplochromis laparogramma, Lithochromis rubripinnis, L. rufus and Haplochromis sp. ‘rockkribensis’, was successful.     

Abundance,distribution, and territory areas of rock-dwelling Lake Tanganyika cichlid fish species

Lake Tanganyika, the second-oldest and second-deepest lake in the world, harbors an impressive cichlid fish fauna counting about 250 endemic species that are characterized by a great level of ecological, morphological, and behavioral specialization. This study describes and compares cichlid fish communities at two rocky shores with differential human impact in the south of Lake Tanganyika. Species inventories and depth-dependent abundances were elaborated. About 41 and 46 sympatric cichlid species were recorded in the two study sites, respectively. Variabilichromis moorii was the most abundant species (29–60% of total number of fishes), followed by Aulonocranus dewindti (3–19%), Tropheus moorii (12%), Ophthalmotilapia ventralis (4–10%), Eretmodus cyanostictus (6–11%), and Cyathopharynx furcifer (0.01–9%). All other species had abundances below 5%. It further emerged that large cichlids such as Petrochromis species, Cyathopharynx furcifer, and Lobochilotes labiatus were very rare at one location, with frequencies of 0.55% or less. Territorial sizes of three particularly abundant species, Variabilichromis moorii, Aulonocranus dewindti, and Tropheus moorii, were assessed by behavioral observations. We distinguished between territorial core areas and total defended area, yielding average core areas between 0.4 (V. moorii) and 1.6 m² (T. moorii), and total defended areas averaging for each species between 1.6 (V. moorii) and 5.0 m² (A. dewindti) with no significant differences between the two study sites. The data on individual densities are also relevant for evolutionary studies, in that they allow more accurate calculations of effective population sizes.     

Interspecific relationships of aufwuchs-eating fishes in Lake Tanganyika

Synopsis On a rocky shore of Lake Tanganyika aufwuchs-eating is practiced by 18 fish species: 17 cichlids and 1 cyprinid. The majority takes mostly either filamentous or unicellular algae.Tropheus moorei and its taxonomically related species most closely resemble one another in diet among the species taking mostly filamentous algae, and thePetrochromis species do so among the species taking mostly unicellular algae.Petrochromis polyodon andT. moorei severely interfere with the feeding activities of related species. These two dominant species share both intensive grazing sites and temporal grazing patterns, and there seems to be a symbiotic relationship between them. Symbiotic relationships are also seen in seven cases of associated feeding by carnivorous fishes. Differences in diet or feeding behavior are found between these symbionts. Small but clear differences are found betweenP. polyodon andT. moorei and between the associating and the carnivorous host fishes in the four cases of associated feeding. These small differences seem attributable to morphological differences and may have been effective for the evolution of symbiotic relationships.Contribution from the Laboratory of Animal Ecology, Kyoto University, No. 461.     

Positive selection and gene conversion in SPP120, a fertilization-related gene, during the East African cichlid fish radiation

The ability to infer historical natural selection from sequence data aides in finding genes that might be important in adaptation and the formation of new species. As the fastest evolving and largest known vertebrate radiation, the cichlid fish of the African Great Lakes exhibit a wide range of recent morphological diversification. We used DNA databases, mostly of expressed sequence tags, to find candidate orthologous coding sequences from 2 tribes of cichlids and, using an automated procedure, scanned these sequence pairs for high dN/dS, the signal of positive selection and protein adaptation. The results included vertebrate genes commonly found to be under selection (e.g., major histocompatibility complex [MHC] loci) as well as genes known to be important specifically in the cichlid radiation (e.g., long-wave-sensitive opsins). Further investigation focused on a gene encoding a fertilization-related protein, SPP120, which was previously known only from cichlids. Using maximum likelihood analysis on novel SPP120 cDNA sequences from a range of African cichlids, we demonstrate the influence of positive selection in a specific subregion of the protein. We also show that SPP120 is a tandemly arranged, multicopy gene evolving with occasional interlocus gene conversion. A search of the Medaka genome database also revealed a tandem arrangement of multiple SPP120 copies and evolutionary rate differences between Medaka gene subregions mirroring those found for cichlids. Combined, these results suggest that SPP120 has been under repeated diversifying selection for over 100 Myr.