The history of fish communities, biodiversity and environment of Lake Victoria and the lessons learnt

The first fishery survey of Lake Victoria was conducted between 1927 and 1928 (Graham 1929). Atthat time, the lake had a diverse fish fauna and the fishery was dominated by two endemic tilapiine cichlids; Oreochromis esculentus (Graham 1929) and O. variabilis (Boulenger 1906). There were a number of other species such as Protopterus aethiopicus Heckel 1851, Bagrus docmac (Forsk.) 1775, Clarias gariepinus (Burchell), Barbus species, mormyrids, Synodontis spp, Schilbe intermedius (Linn.) 1762 and Rastrineobola argentea Pellegrin, 1904 that were also abundant in the lake most of which made a significant contribution to the fishery (Graham 1929, Worthington 1929, 1932, Kudhongania & Cordone 1974). Haplochromine cichlids were represented by at least 300 species more than 99% of them endemic (Greenwood, 1974; Witte et al., 1992 a & b). The fishery of Lake Victoria was similar to that of lakes Kyoga and Nabugabo (Worthington 1929; Trewavas 1933; Greenwood 1965, 1966; Beadle 1962, 1981). There were also important fisheries on the inflowing rivers of Lake Victoria, the most important of which were Labeo victorianus and Barbus altianalis (Cadwallader 1965). The small sized species notably Rastrineobola argentea and haplochromines cichlids were not originally commercially exploited.

Composition, biomass, distribution and population structure of the fish stocks

Until the 1970s, Lake Victoria had a multi-species fishery dominated by the tilapiine and haplochromine cichlids. There were important subsidiary fisheries for more than 20 genera of non-cichlid fishes, including catfishes (Bagrus docmak, Clarias gariepinus, Synodontis spp and Schilbe intermedius), the lungfish (Protopterus aethiopicus) and Labeo victorianus) (Kudhongania and Cordone 1974). Stocks of most of these species declined and others disappeared following the introduction of four tilapiines (Oreochromis niloticus, Oreochromis leucostictus, Tilapia rendalli and Tilapia zillit) and Nile perch (Lates niloticus) during the 1950s. Since then the commercial fishery in the Uganda portion of Lake Victoria has been dominated by the Nile perch, Nile tilapia (Oreochromis niloticus) and the native cyprinid species, Rastrineobola argentea (Mukene).

Fish species diversity in the Victoria and Kyoga lake basins: their conservation and sustainable use

Introduction of exotic fish species especially the Nile perch Lates niloticus, is believed to be responsible for the decline of fish species diversity in lakes Victoria, Kyoga and Nabugabo.About 60% of the haplochromine cichlids are thought to have become extinct from L. Victoria due to predation by the Nile perch. However there are many lakes satelite to the lakes Victoria and Kyoga basins which still have fish fauna similar to that of the main lakes. many of the satellite lakes are separated from the main lakes in, which Nile perch was introduced by extensive swamps that provide a barrier to Nile perch .A survey was carried out in a number of these satelite lakes and an inventory made of existing fish species. Their distribution and relative abundances were also determined. The lakes studied included Nawampasa, Nakuwa,Kawi Lamwa Gigate, Nyaguo, Agu, Nabugabo. Kayanja, Kaytigi, Mburo, Kachera and Wamala.Some habitats within the main lakes Victoria and Kyoga, especially those with rocky outcrops· and macrophyte cover that provide refugia for endangered species from Nile perch,were also surveyed) Various stations along the River Nile were also sampled to quantify the fish species that are still resent. Kyoga minor lakes were found to have the highest number of fish species especially of haplochromine cichlids. Many haplochromine trophic groups that were thought to be extinct from 1. Victoria still occur in these lakes.!Some of the satellite lakes, especially lakes Kayugi, Mburo and Kachera still contain .healili populations of oreochromis. I esculentus that could be used as brood stock in fish farming. Many of these lakes should .I ( I therefore be protected for conservation offish species diversity

Genetic status of selected fish taxa in relation to conservation of genetic and species diversity in the Victoria and Kyoga Lake basins

Cichlids are known for their explosive radiation especially in the African Great Lakes marked with a high level of lake endemism. These fishes have been characterized mainly along trophic and habitat differences, by variation in morphological structures such as teeth and jaws and by differences in body shape and coloration. Cichlids are important as a microcosm of macroevolution. The explosive radiation, young evolutionary scale, and the isolation of groups characterized with high levels of endemism and presence of living fossils makes the group important for evolutionary and genetic studies. Lake Victoria region cichlids which are isolated and relatively more recent in evolution were the last to be appreciated in their diversity. Recently Ole Seehausen has found scores of rock fishes in Lake Victoria which were up to then thought to be absent from the Lake and only known to occur in Lakes Malawi and Tanganyika. Greenwood put together the species groups of Lake Victoria, and later in the early 1980's revised the classification of haplochromine species to reflect the phyletic origin and interrelationship of the various groups in Lake Victoria region. Melan Stiassny has been interested in early evolution of cichlids while the likes of Paul Fuerst and Lees Kaufman and Axel Meyer have been interested and are working to explain the speciation mechanisms responsible for the explosive radiation and evolution of cichlids. Locally S.B Wandera and his student Getrude Narnulemo are spearheading the biodiversity and taxonomic studies of cichlids in Lake Victoria region

The biology, ecology, distribution and conservation of some surviving native non-cichlid fish species of Lakes Victoria, Kyoga and Nabugabo

Prior to introduction of non-native fish species into Lakes Victor i a, Kyoga and Nabugabo, the three lakes suppor ted diverse fish fauna representing 13 families consisting of six cichlid genera and fifteen non-cichlid genera. There were about 50 non-cichlid species and over 300 cichlids consisting of mainly haplochromines (Graham 1929, worthington 1929, Greenwood 1960). Many of the species were commercially and scientifically important and provided a rich variety of protein source to choose from. Following introduction of the Nile perch and several tilapiines species, most of the native species were drastically reduced and some have apparently disappeared. The few remaining species appear to be restricted in distribution due to the presence of the Nile perch. They are mainly confined to refugia such as marginal macrophytes, rocky outcrops and small satellite lakes which are separated from the areas of introduction by swamps

The role of Yssichromis species (Pisces: Cichlidae) in the trophic ecology and foodwebs of Lake Victoria

Many haplochromine cichlids coexisted in Lake Victoria before the upsurge of Nile perch. The introduction of the Nile perch led to depletion of many haplochromines and other fish species in Lake Victoria. The impact of Nile perch predation on haplochromines differed for different haplochromine trophic groups. Yssichromis fusiformis (G) and Yssichromis laparogramma (G) are among the species that have survived in the lake. Yssichromis spp. was studied with the aim of determining their trophic role, food and feeding habits. Samples were collected from Bugaia, Buvuma channel and Napoleon Gulf in the northern part of Lake Victoria. The food of Yssichromis spp. varied with size of fish. Both Y fusiformis and Y laparogramma fed on Copepods, Cladocerans, Chaoborus and Chironomids. Juvenile Yssichromis spp. fed exclusively on zooplankton comprising Cyclopoid copepods, Calanoid copepods and Cladocera. The relative importance of Chironomid larvae and Calanoid copepods was higher in Bugaia than in Buvuma channel while Cyclopoid copepods and Chironomid pupae were relatively less important in Bugaia. The main food items that Yssichromis spp. fed on in Buvuma channel were Chironomid larvae Cyclopoid copepods, Cladocerans and Calanoid copepods. In Napoleon Gulf, fish caught from commercial fishery of Rastrineobola argentea (P) had fed on Chaoborus and Chironomids. Overall, Yssichromis spp. fed on more zooplankton in Buvuma than in Bugaia. Yssichromis spp. and R. argentea are presently the most abundant zooplanktivores in the northern part of Lake Victoria and are playing an important trophic role as major consumers of zooplankton and insect larvae in the foodweb of the lake ecosystem. Yssichromis spp. are bridging the transfer of energy from the lower to the higher trophic levels as secondary consumers. The fishery is still not contributing to the direct conversion of the primary products, the phytoplankton and detritus that were efficiently utilised by the diverse haplochromine trophic groups that existed before the Nile perch boom.

Changes in fish fauna and the impact of the introductions on fish yield

There have been considerable changes in fish species composition in Lakes victoria, Kyoga and Nabugabo since the Nile perch were introduced. Populations of most of the native species have declined and many species may have become extinct. The original decline in the fish stocks was due to overfishing but the recent and more drastic decline has been attributed to predation by the Nile perch. Nile perch feeds on invertebrates changing to a piscivorous diet with size. Haplochromine cichlids, which were the most abundant fish in Lakes Victoria just before the Nile perch populations started increasing rapidly have been depleted. As more suitable types of prey were depleted in the new habi tats, Nile perch switched to other prey types to the extent of feeding even on its own young. There are, fears that the Nile perch will overshoot its food supply, resulting in a reduction of its own population and subsequently a collapse in the fishery (FAD 1985).

A report of the gillnet survey in the Ugandan waters of Lake Victoria under IFMP (January to March 2006)

Under the Implementation of the Fisheries Management Plan (IFMP) for Lake Victoria Result area 4, quarterly gillnet surveys are undertaken to monitor changes in fish stocks and environmental parameters in the shallow nontrawlable areas of the lake For purposes of monitoring surveys, the Ugandan sector of Lake Victoria is divided into 3 zones as shown in Figure 1. During the second quarter of APE2, two gillnet surveys were undertaken in zones 1 and 3 in February and March 2006 respectively. The purpose of the surveys was to monitor changes in the fish stocks and their biological characteristics, water quality, algal dynamics and invertebrate communities; as detailed in the various sections of the report. The surveys followed those conducted in November and December 2006 in the same zones. Results of the surveys showed that the number of fish taxa was higher in the near-shore fleets (0-100m) decreasing towards offshore. The near-shore areas were also associated with high primary productivity and hence secondary production to which Caridina and other invertebrates are part. These organisms are an important source of food for the fish and this may partly account for the high number of fish species recorded in this area of the lake. It was also observed that although Nile perch was the most dominant fish species recorded in all the stations during the surveys, haplochromines, Brycinus sadleri, Brycinus jacksonii Oreochromis niloticus and various mormyrid species contributed significantly to the fish biomass. The presence of many fish species and their coexistence with the predator, Nile perch is attributed to the presence of macrophyte cover and rocky habitats which serve as refugia in the shallow inshore habitats of Lake Victoria. In addition, the vegetated habitats are an important source of food for the fishes. As reported in macro-invertebrate studies, big populations of Caridina and other invertebrates were recorded among macrophyte beds. Caridina is an important source of food for juvenile Nile perch and other fish species so are the other invertebrates especially chironomid larvae, odonata nymphs and molluscs. Resurgence in haplochromine cichlids was observed during the surveys. The presence of haplochromines cichlids in all the sites especially Thruston Bay where it ranked the second by percentage contribution in number, is evidence of the recovery of this group of fishes which had declined largely due to predation by L. niloticus. Caridina nilotica has also increased in biomass and is a major component of the Nile perch diet. This could have reduced predation pressure on the haplochromines by Nile perch and has possibly contributed to recent resurgence in haplochromines cichlids in the lake in the shallow nontrawlable areas of the lake Rastrineobola argentea was found to be an important prey item for Nile perch and other fish species such as Clarias gariepinus. Measures should therefore be taken to ensure sustainable harvesting of Dagaa so that there is enough left to sustain the fishery of Nile perch and other species.

The role of satellite lakes in conservation of fish species diversity in the Lake Kyoga basin

Lakes Victoria and Kyoga had, a diverse fish fauna, which was important as food for local population and valuable in scientific studies. Over the past twenty years, the diversity of fish in these lakes had declined due to over-exploitation, introduction of new fish species including the piscivorous Nile perch and degradation of fish habitat. Studies of satellite lakes in the Victoria and Kyoga lake basins suggested that some of these lakes harboured species which had been lost from the main lakes. In order to better understand the extent, to which these satellite lakes may serve as refugia, a faunal survey was undertaken to determine the distribution and nature of the taxa found. Seven satellite lakes and the eastern end of the main Lake Kyoga adjacent to these minor lakes were surveyed over a two-year period for fish species diversity. A total of 68 fish species were recorded of which 41 were haplochromines. Almost all the native non cichlids which occurred in the main lakes (Victoria and Kyoga) before the Nile perch upsurge recorded. Lakes Nawampasa, Gigati, Kawi, Agu and Nyaguo had the highest fish species and trophic diversity. The trophic diversity of haplochromines (based on Shannon Weaver Index) was highest in Lake Nawampasa (1.28), followed by Gigati (1.25), Kawi (1.18), Agu (0.8), Lemwa (0.81), Nyaguo (0.35) and was lowest in the main Lake Kyoga. Potential threats to these lakes were from collectors of ornamental fish species, especially the haplochromines, the spread of the predatory Nile perch and the water hyacinth, which are already in Lake Kyoga, and the destruction of macrophytes through harvesting of papyrus and reclamation for agriculture. The human population around these lakes harvested the fishes for food but the levels of exploitation were still low because the lakes were adjacent to main Lake Kyoga, the major supply of fish. Ornamental fish dealers were encouraged to start captive breeding of the fish for export to reduce pressure on the lakes and demonstrations for breeding were set up at FIRI in Jinja. Meetings and seminars were held with some of the communities living around the lakes sampled and the importance of fish species found in these lakes and the dangers of destructive practices discussed. Representatives of all taxa of fish caught from the lakes were preserved, catalogued and stored in the FIRI Museum. Results from this survey support the motion that these satellite lakes are important refugia for endemic diversity. Based on survey, we recommend that SaIne of these lakes like Nawampasa, Gigati, Kawi, Agu and Nyaguo could be designated as conservation areas of species threatened in the main lakes. One of the factors that seem to have prevented the spread of Nile perch into Kyoga Minor lakes seems to have been the presence of extensive swamps around these lakes and the low oxygen levels that exist in these habitats. Clearing of swamps and vegetation that separate Kyoga minor lakes from the main lake should be avoided to prevent Nile perch from spreading into these lakes.

Rapid behavioral and genomic responses to social opportunity.

From primates to bees, social status regulates reproduction. In the cichlid fish Astatotilapia (Haplochromis) burtoni, subordinate males have reduced fertility and must become dominant to reproduce. This increase in sexual capacity is orchestrated by neurons in the preoptic area, which enlarge in response to dominance and increase expression of gonadotropin-releasing hormone 1 (GnRH1), a peptide critical for reproduction. Using a novel behavioral paradigm, we show for the first time that subordinate males can become dominant within minutes of an opportunity to do so, displaying dramatic changes in body coloration and behavior. We also found that social opportunity induced expression of the immediate-early gene egr-1 in the anterior preoptic area, peaking in regions with high densities of GnRH1 neurons, and not in brain regions that express the related peptides GnRH2 and GnRH3. This genomic response did not occur in stable subordinate or stable dominant males even though stable dominants, like ascending males, displayed dominance behaviors. Moreover, egr-1 in the optic tectum and the cerebellum was similarly induced in all experimental groups, showing that egr-1 induction in the anterior preoptic area of ascending males was specific to this brain region. Because egr-1 codes for a transcription factor important in neural plasticity, induction of egr-1 in the anterior preoptic area by social opportunity could be an early trigger in the molecular cascade that culminates in enhanced fertility and other long-term physiological changes associated with dominance.

Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times

Background: After a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (~20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation.
Results: Gene coalescence analyses [11 microsatellite loci and mitochondrial DNA (mtDNA) sequences] suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thin- and thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (d15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thin- and thick-lipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001).
Conclusions: This study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification.

Parsing parallel evolution:Ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua

The study of parallel evolution facilitates the discovery of common rules of diversification. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex) - from two Great Lakes and two crater lakes in Nicaragua - to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expression in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underexpressed in the thick-lipped morph across all four lakes. However, other aspects of lips' gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (dC and dN) differ between all sympatric morphs, with the greatest differentiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution. © 2012 Blackwell Publishing Ltd.

Identity of a Tilapia Pheromone Released by Dominant Males that Primes Females for Reproduction

Knowledge of the chemical identity and role of urinary pheromones in fish is scarce, yet it is necessary in order to understand the integration of multiple senses in adaptive responses and the evolution of chemical communication [1]. In nature, Mozambique tilapia (Oreochromis mossambicus) males form hierarchies, and females mate preferentially with dominant territorial males, which they visit in aggregations or leks [2]. Dominant males have thicker urinary bladder muscular walls than subordinates or females and store large volumes of urine, which they release at increased frequency in the presence of subordinate males or preovulatory, but not postspawned, females [3–5]. Females exposed to dominant-male urine augment their release of the oocyte maturation-inducing steroid 17α,20β-dihydroxypregn-4-en-3-one (17,20β-P) [6]. Here we isolate and identify a male Mozambique tilapia urinary sex pheromone as two epimeric (20α- and 20β-) pregnanetriol 3-glucuronates. We show that both males and females have high olfactory sensitivity to the two steroids, which cross-adapt upon stimulation. Females exposed to both steroids show a rapid, 10-fold increase in production of 17,20β-P. Thus, the identified urinary steroids prime the female endocrine system to accelerate oocyte maturation and possibly promote spawning synchrony. Tilapia are globally important as a food source but are also invasive species, with devastating impact on local freshwater ecosystems [7, 8]. Identifying the chemical cues that mediate reproduction may lead to the development of tools for population control [9–11].

Disturbance chemical cues determine changes in spatial occupation by the convict cichlid Archocentrus nigrofasciatus

I studied the effect of disturbance chemical cues on fish that make trade-offs between foraging in an open area and remaining in a safe refuge. I used convict cichlids Archocentrus nigrofasciatus that were either visually exposed to a predator (n = 8) or exposed to water conditioned by chemical cues from disturbed conspecifics (n = 8). Fish visually exposed to a predator decreased their ingestion rate and spent more time in the refuge than in the foraging area, while fish receiving water from frightened conspecifics did not alter their ingestion rate or time spent in the refuge and foraging site, but increased their spatial occupation (i.e., motion). These results suggest that convict cichlids recognized the predator by visual cues. Moreover, disturbance cues are a form of threatening public information that may increase fish spatial occupation due to increased exploring behaviour; but is not sufficiently alarming to alter feeding or increase refuge use. (C) 2004 Elsevier B.V. All rights reserved.

Time-place learning in individually reared angelfish, but not in pearl cichlid

Time-place learning based on food association was investigated in the cichlids angelfish (Pterophyllum scalare) and pearl cichlid (Geophagus brasiliensis) reared in isolation, therefore eliminating social influence on foraging. During a 30-day period, food was placed in one side of the aquarium (containing three compartments) in the morning and in the opposite side in the afternoon. Learning was inferred by the number of correct side choices of all fish in each day of test (15th and 30th). During the test day fish were not fed. The angelfish learned to switch sides at the correct day period in order to get food, suggesting this species has time-place learning ability when individually reared. on the other hand, the same was not observed for pearl cichlid. (c) 2006 Elsevier B.V. All rights reserved.