Fisheries and Cichlid Evolution in the African Great Lakes: Progress and Problems

131 Article

Fisheries and cichlid evolution in the African Great Lakes: progress and problems

Rosemary Lowe-McConnell St George’s Park, Burgess Hill, Sussex RH15 0SG, UK. Email: [email protected]

Received 22 May 2009; accepted 25 September 2009; published 16 November 2009

Abstract

This paper updates Recent Advances in the African Great Lakes: Fisheries, Biodiversity and Cichlid Evolution published by the Freshwater Biological Association in Freshwater Forum (Lowe- McConnell, 2003). Since 2003 many international teams have continued research on lakes Malawi, Victoria and Tanganyika. This review discusses the decline of the important commercial fisheries in all three lakes, together with changes in ecological and limnological conditions which the fishes now face. It also describes advances in our understanding of how the spectacular flocks of endemic cichlid species have evolved in each lake and continue to coexist.

Keywords: African lakes; cichlid evolution; cichlid ecology; fisheries; Lake Victoria; Lake Malawi; Lake Tanganyika.

Introduction obtain funds for projects on lakes Malawi, Tanganyika and Victoria. These lakes were all facing serious threats The East African Great Lakes have long been renowned for caused by the rapid rise in human populations, with fisheries of vital importance for the rapidly rising riparian associated over-fishing, sedimentation, and pollution from human populations and as biodiversity hotspots with changes in land use in the lake basins. Since the early 1990s spectacular endemic faunas. The flocks of cichlid fishes research involving over a hundred scientists, financed unique to each of the three largest lakes, Victoria (69 000 by many international bodies, has produced numerous km2) and the long deep rift-valley lakes, Tanganyika and publications in widely-scattered journals. In 2003, the Malawi (previously Nyasa) (Fig. 1), have offered unique Freshwater Biological Association published a Special opportunities to investigate how new species evolve and Issue of Freshwater Forum on Recent Advances in the African coexist (as discussed by Lowe-McConnell, 1993, 1996). Great Lakes: Fisheries, Biodiversity and Cichlid Evolution In 1989, an International Symposium on ‘Resource Use (Lowe-McConnell, 2003). This synopsis summarised the and Conservation of the African Great Lakes’ was held at status of the fisheries and the then current ideas on how Bujumbura on Lake Tanganyika, followed by numerous the rich endemic fish faunas had evolved. It also described workshops at other venues. Further international interest the biodiversity surveys made in each lake based on in biodiversity, generated at the Rio Earth Summit in 1992, underwater (SCUBA) observations of fish ecology and then enabled the United Nations and other agencies to behaviour, followed by cichlid breeding experiments in

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 © Freshwater Biological Association 2009 132 Lowe-McConnell, R.

Fig. 1. The East African Great Lakes: Lake Victoria drains via Lake Kyoga and Lake Albert to the Nile, Lake Tanganyika to the Congo system (Zaire) and Lake Malawi to the Zambezi River. Figure originally from Lowe-McConnell, R. 1996. Fish communities in the African Great Lakes. Environmental Biology of Fishes, 45: 219-235. Reproduced with kind permission of Springer Science and Business Media. aquaria and DNA techniques in many laboratories to test ideas on the evolution, origins and relationships of the Fisheries cichlid species. New publications since 2003 have further advanced our understanding of how the spectacular Lake Malawi fisheries flocks of cichlid species have evolved and coexist in lakes Victoria and Malawi, but the main commercial fisheries Sixty years ago the first fishery survey of Lake Nyasa (now of these lakes, so needed to feed the rapidly rising human L. Malawi) showed that the main commercial fisheries populations, have declined. The present review describes were supported by cichlid tilapia caught in shore seines the most outstanding contributions on both these topics and open water ring nets (Bertram et al., 1942). Since published from 2003 to 2009. then, however, tilapia abundances have declined and the

© Freshwater Biological Association 2009 DOI: 10.1608/FRJ-2.2.2 Fisheries and cichlid evolution in the African Great Lakes 133 species of endemic tilapia are now so scarce that the main could adversely affect Malawi’s endemic fishes, as it did commercial fishery (Maldeco, which works in association when introduced into Madagascar (Reinthal et al., 2003). with the Malawi Fishery Department) has resorted to Research into environmental conditions affecting fish breeding tilapia in fish-farm ponds to stock large enclosures production in Lake Malawi has included, for example, fixed in open waters in the south east arm of the lake. the work by Duponchelle et al. (2005) on food partitioning Here they rear endemic tilapia (Oreochromis shiranus and within the species-rich benthic fish community. Using a ‘chambo’ O. karongae) but the endemic, more open-water- combination of stable isotopes and stomach analyses, they dwelling O. lidole, once so abundant in ring net catches, has found that, although benthic algal production contributed been over fished to such an extent that it has now vanished to the energy requirements of offshore fishes living in and is ‘probably extinct’ (Turner, personal communication). water 10 m to 30 m deep, the larvae of the abundant lake Maldeco, which produces 70 % of Malawi’s total fish catch, fly Chaoborus edulis were the most important food source no longer targets tilapia (the most popular fish) which was for demersal fishes, thus supporting the hypothesis reported in 2005 to be at the ‘lowest point ever’. Artisanal that demersal fish production in L. Malawi is sustained fisheries for cichlids and other fishes continue elsewhere on mainly through the pelagic food chain, rather than from this 600 km long lake, from which total catches are reported benthic detritus. Isotopic differences among species by the Malawi Fisheries Department to fluctuate between with apparently similar diets, feeding behaviour and 26 000 and 47 000 tonnes annually. To augment the fish depth preferences, suggested that important resource supplies Maldeco uses three bottom trawlers which catch partitioning does exist among L. Malawi’s benthic mainly very numerous small haplochromine cichlid species, haplochromine cichlids. A Special Issue of the Journal of including ndunduma Diplotaxodon of several species, Great Lakes Research on The African Great Lakes (eds Bootsma discovered during the UK/SADC Pelagic Zone survey in et al., 2003), has an introductory paper by Bootsma & 1995. Small cichlid species now contribute between 60 % Hecky (2003) comparing the biology and limnology of and 70 % of Maldeco’s annual catch, of which 90 % is sold the African Great Lakes. Twelve of the other very diverse fresh (frozen); Maldeco also has a fish processing plant and papers were based on data from L. Malawi. These, in smoke kiln for fillets of any large fish they catch, especially addition to discussing seasonal and spatial patterns of catfishBagrus meridionalis. To help meet the country’s large experimental trawl catches (Deponchelle et al., 2003) demand for fish, they have acquired another landing site at and the return to local fisheries management (Dobson & Salima on the main lake, for which a fourth fishing vessel is Lynch, 2003), included other observations by numerous on order (Press Corporation Ltd, 2009). authors on meteorology, nutrient upwelling, sources Fish from smaller lakes in Malawi, and from pond and fluxes of organic carbon, silica cycling, community culture, also contribute to the country’s total catch. The composition, distribution and nutrient status of epilithic WorldFish Centre, based in the Philippines, has assisted periphyton in the rocky littoral, environmental factors Malawian farmers to grow tilapia in rain-fed ponds for controlling the distributions of benthic invertebrates on which new varieties of tilapia are being selected for fast rocky shores, and nitrogen and phosphorus regeneration growth. Commendably, Malawi does not stock exotic fish, by cichlids in the littoral zone. In a paper on the impact which can so easily escape to the detriment of indigenous of land use on sediments and nutrients, Hecky et al. species. The very vigorous Nile tilapia (O. niloticus), (2003) showed that changes in land use in the L. Malawi cultivated in many ponds worldwide, when introduced into basin, with its rapidly increasing human population and Lake Victoria ousted the endemic tilapia (as described later). associated agricultural development and forest clearance, This aggressive species has now spread in southern Africa, probably increased nutrient loading to the lake by 50 %. including Lake Kariba from where it has replaced Zambezi Responses to nutrient-enrichment experiments tilapias (Tweddle, 2007). This very dominant tilapia species (with P, N and Fe) demonstrated that, in adequate light,

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 134 Lowe-McConnell, R. phytoplankton quickly become nutrient-deficient. O. niloticus thrived despite the presence of this predatory Enrichment experiments with and without zooplankton centropomid (now Latidae) that was introduced into the (> 50 µm) by Guildford et al. (2003) in Lake Malawi Ugandan waters of the lake in the mid 1950s as a ‘sport’ fish (during three seasons – stratified rainy, deep mixing and and to crop the numerous small haplochromine species. stratified dry) demonstrated that, when light is adequate, phytoplankton in containers quickly become nutrient- The rise and fall of Nile perch populations deficient. When Fe was added with N and P, the response The HEST (Haplochromis Ecology Survey Team) measured as chlorophyll was four times the response team from Leiden University, which has reviewed the without Fe. Light was a factor controlling phytoplankton chronology and causes of the Nile perch invasion in Lake growth in situ during the deep mixing season. Grazer Victoria (Goudswaard et al., 2008) record how Nile perch experiments demonstrated that zooplankton (> 50 µm) were unofficially introduced into Ugandan waters of Lake are important in modifying the response of algae to Victoria in August 1954 by the Game & Fisheries Department light and nutrients. In Lake Victoria, experiments had (Amaras, 1986). This followed the Department’s pre-1960 demonstrated that phytoplankton were primarily introduction of Nile perch into Lake Kyoga, into which limited during the early stratified season; increased L. Victoria flows (Kinlock, 1972; Jackson, 2000; Pringle, light levels resulted in N deficiency. The addition of Fe 2005). In May 1960, fishermen reported the first Nile perch stimulated N uptake in both lakes Victoria and Malawi. from gillnet catches near Jinja; seven others caught near there in the same year were subadults of 28 cm to 43 cm in Lake Victoria: the present state of the length. Several years later Nile perch were caught in Kenya, fisheries then in low densities lake-wide in 1969–1970. In Tanzanian waters large numbers of sub-adults and adults appeared in Tilapia in Lake Victoria 1983, while juveniles were first seen there in 1985. In Lake Victoria the endemic tilapia (O. esculentus and Catches of haplochromines in trawl nets had started O. variabilis), here caught mainly by gillnets, were also the to decline shortly after the onset of the commercial trawl basis for the first commercial fisheries. Tilapia catches fishery, reputedly due to intensive fishing, but their declined as fishing effort intensified in the three riparian final disappearance occurred after the Nile perch boom countries (Kenya, Uganda and Tanzania) as the human and despite the abandonment of the commercial trawl population increased. In the mid-1950s, in an attempt to fishery in 1986. HEST also suggested that this decline of boost catches, Tilapia zillii, a macrophyte-feeding species, the haplochromines (which included loss of the large, was introduced from Lake Albert in western Uganda. As predatory species) had, by decreasing predation on, and an inshore dweller it was thought that this species would competition with, juvenile Nile perch, paved the way for not interfere with the endemic tilapias and would help to the successful reproduction of those Nile perch that had clear swamps. However, with it came O. leucostictus and immigrated. Perhaps over-exploitation of haplochromine Nile tilapia O. niloticus (Lowe-McConnell, 1990, 2006). The cichlids in the 1970s in the Nyanza Gulf in Kenya might latter, introduced from other Ugandan lakes, has now have played a similar role. Once their densities were high, replaced (possibly with some hybridisation) the endemic pioneering sub-adult Nile perch might have effected a O. esculentus; O. variabilis is now rare in catches from the change in the species composition by the eradication lake (probably affected by the introduction of T. zillii). of haplochromines in favour of juvenile Nile perch. The smaller O. leucostictus, found in swampy places, are Nile perch had also been introduced earlier into commercially unimportant. Goudswaard et al. (2002) Lake Kyoga, into which Lake Victoria drains before it reviewed the status of the tilapiine fish stock before and after the continues over the barrier of the Murchison Falls into upsurge of Nile perch (Lates niloticus) in Lake Victoria, where Lake Albert. Lake Kyoga had a Nile perch boom about

© Freshwater Biological Association 2009 DOI: 10.1608/FRJ-2.2.2 Fisheries and cichlid evolution in the African Great Lakes 135 a decade earlier than L. Victoria, when the total fish countries. Catch statistics indicate that fish landings of yield increased from 18 000 tonnes in 1964 to 167 000 t ca. 100 000 t per year rose to ca. 500 000 t annually in the in 1978, largely due to a rise in Nile perch catches from early 1990s, just after the Nile perch boom when this species 700 to 71 000 t. This was followed by a fall in Nile perch formed more than 70 % of the catch. During the 1990s the catches to 15 000 t in 1989. By 2006, L. Kyoga’s estimated establishment of so many processing plants around the total catch of 34 700 t consisted of 15 % Nile perch, 44 % lake led to a depletion of Nile perch catches through over Rastrineobola argentea, 28 % the introduced O. niloticus, fishing. The factories now have a total capacity of 420 t per together with native lungfish Protopterus aethiopicus, some day, but many operate well below capacity. In 2003 the haplochromines, and catfishes Clarias gariepinus and estimated catch was worth at least US$ 540 million at the Bagrus docmac. The haplochromine species that had almost fish landings, plus a large sum earned by fish exports from disappeared showed signs of recovery (Witte et al., 2009). each of the three countries, and over a million people were Lakes George and Edward, in western Uganda, once directly or indirectly dependent on the lake fishery. had one of the most productive fisheries for indigenous To gather information on the fish stocks, the ecology O. niloticus, the main commercial fishery for Nile tilapia of the commercial species, and social and economic supporting the TUFMAC fish factory on L. George, with aspects of management – all necessary for the fisheries to catches fluctuating around 2700 t a year. This had to close be sustainable – a Lake Victoria Fisheries Research Project in the late 1970s due to the decline in size of tilapia caught, (LVFRP) was set up. This worked in close association together with political difficulties affecting transport and with Uganda’s Freshwater Resources Research Institute increased poaching, which all exacerbated the decline (formerly EAFFRO (East African Freshwater Fisheries of this once very profitable fishery (Lowe-McConnell, Research Organisation); Lowe-McConnell, 2003), based 2006). Nile perch are absent from the L. George fish in Jinja. The LVFRP – a consortium of the Hull (UK) fauna so were not responsible for the decline in catches International Fisheries Institute in collaboration with the there. In the 1990s lakes George and Edward produced Fishery Research Institutes of Uganda, Kenya and Tanzania over 11 000 t of fish a year for Uganda, but catches now and a renewed Lake Victoria Fisheries Organisation – was have a much smaller proportion of O. niloticus together also based in Jinja. The stock assessment from 1997–2001 with catfishes and lungfishProtopterus ( ). These lakes for Tanzanian waters, with comparative references for ultimately flow into Lake Albert, via the Semliki River, Ugandan and Kenyan waters (Mkumbo et al., 2007), linked whose indigenous Nile perch are part of its nilotic fish both fisheries-independent data from bottom trawl surveys, fauna and where very few haplochromine species have and fisheries-dependent data to growth, mortality and evolved (see Lowe-McConnell, 1987). Commercial catches reproductive characteristics of the stock. The 2000 frame from L. Albert are mainly of large characins and catfishes. survey had revealed an intensive fishing effort and the Nile perch fishery was found to depend largely on juvenile fish; The Lake Victoria Fisheries Research Project male Nile perch first matured at 54 cm total length (TL) (1.6 (LVFRP) years old) and the females at 76 cm TL (2.5 years old). Over HEST’s routine trawl samples had shown that as the Nile 80 % of the commercial catch was below the maturation perch population erupted ca. 200 endemic haplochromine size for males and 99 % below that for females. Bottom species vanished from the Tanzanian waters of Lake Victoria trawl data (88 % juveniles) suggested good recruitment (as discussed later), a loss of biodiversity that horrified to the stock, but modelling of yield per recruit indicated biologists internationally. But, in time and with factories unsustainable tendencies. From LVFRP studies the annual set up to purchase and freeze fillets, the originally despised yield was estimated to be 138 324 t, well above the estimated Nile perch became the most important commercial fish, sustainable level of 109 000 t. They therefore recommended supporting a valuable export trade from all three riparian that the exploitation rate should be reduced by 50 %, and

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 136 Lowe-McConnell, R. for Nile perch the size at first capture should be increased. in algal biomass. After re-examining the LVFRP stock- Co-management was considered to be the most effective assessments (all based on classical steady-state models) option to implement monitoring, control and surveillance. this team concluded that claims of over fishing of the A management plan was set up to harmonise fishery lake are not valid, as fish biomass, catch rates and size policies in the three riparian countries. This adopted structures have remained stable over the last 30 years. lake-wide regulations and a co-management approach, The resilience of the lake’s fish stocks as a whole could with 160 Beach Management Units (BMUs) arranged on only be explained by intensified biological productivity fish landing sites around the lake. The harmonised rules due to eutrophication. Algal production in the lake has included banning beach seines and bottom trawls, cast been shown to be light-limited and an upper level of nets, gill nets of mesh less than 130 mm (5 inches), and a production has been reached, so there is a danger that the slot size of 50 cm to 85 cm TL for Nile perch. Sadly (and eutrophication process will reverse into an accelerated perhaps understandably) some violence was reported process of decay. The immediate threat to L. Victoria from a few Ugandan beaches between the locally elected is, in their view, not over fishing but eutrophication, BMU officials and the fishermen whose gear they and management should, therefore, be more concerned confiscated (Cowx, personal communication). Other with controlling eutrophication than focusing on ‘illegal LVFRP studies included a sociological investigation of fishing practices that have no significant effect on fish why hunger and malnutrition still exist among some of the stocks’. As Turner (1996) had pointed out, the decision lakeshore peoples despite income from the valuable Nile on whether to manage lakes in a way which maximises perch fishery. Geheb et al. (2007) found that the fishermen yields (for local food) or profits is essentially political; who receive the earnings from the Nile perch processing fisheries based on large predators (such as Nile perch) factories fail to pass them on to the women who are may be more profitable in the short term, but those based responsible for feeding their families, hence the increasing on the smaller, short-lived species can give greater yields. level of malnutrition observed in lakeside villages. The small endemic pelagic cyprinid, dagaa (Rastrineobola Limnological conditions affecting fisheries in argentea) has become the second most important commercial Lakes Victoria and Malawi species in Lake Victoria since the decline of Nile perch, The Special Issue on The African Great Lakes (eds Bootsma so its biology and distribution in the lake was examined et al., 2003) has, in addition to the papers on Lake Malawi to formulate a rational exploitation and management plan already discussed, several papers on Lake Victoria. for this species. From five acoustic surveys made between Stable isotope analyses of nitrogen and carbon values in 1999 and 2001, combined with bottom and pelagic frame biota have proved a powerful tool with which to study trawl surveys, the mean total biomass of R. argentea in the trophic position and dietary sources of the L. Victoria lake was estimated as 476 902 t, the majority of which was fishes (Campbell et al., 2003a). Data on stable isotope distributed in waters more than 40 m deep. The biomass analyses of food web structure in fish diets, comparing increased progressively over the survey period as Nile those from Winam Gulf (Kenya) and Napolean Gulf perch predation decreased (Tumwebaze et al., 2007). (Uganda), illustrated a short food web with the top But how reliable were the catch statistics? Another predator, Nile perch, feeding on a restricted set of fish, team (Kolding et al., 2008), in an attempt to understand macroinvertebrates and their own juveniles. There was feedbacks in the whole ecosystem, re-analysed fish catch an increase in both N and C values with fish size, showing records from Lake Victoria in relation to limnological how piscivory increases and reliance on invertebrates changes in the lake where the tripling of the human decreases as Nile perch mature. Nile tilapia, in contrast, populations had led to a doubling of nutrient input and feed at lower trophic levels in littoral water. The small, primary productivity, resulting in a 6- to 10-fold surge pelagic cyprinid, Rastrineobola, and the haplochromine,

Haplochromis laparograma had surprisingly high N values, than in benthic species, and highest in the largest fish not consistent with isotopic values of their assumed prey, within each species. The Hg–nitrogen isotope relationship probably reflecting other planktivore invertebrates in their in L. Malawi food webs was comparable to those found diets, such as lake flies (chironomids and chaoborids). The in temperate and arctic lakes, suggesting that the Hg basal stable isotope values were found to be different in the accumulation in freshwater food webs is independent of two gulfs, reflecting the different hydrological conditions climate change and species composition. In L. Victoria, – Winam (Nyanza) Gulf is a shallow, mesotrophic to Campbell et al. (2003b) found total water mercury (THg) eutrophic gulf nearly closed off from the main lake, while concentrations ranged from 1.75 ng L-1 to 5.8 ng L-1, while the Napolean Gulf is in the vicinity of the Buvuma Channel methylmercury (MeHg) concentrations ranged from leading from the main lake to the source of the Nile near 0.2-1 ng L-1. Concentrations of mercury in the water Jinja. Despite the differences in overall values for N and C were higher here than in temperate great lakes, but the at the base of the food web, food web structures were very top fish predator, Nile perch, had relatively low THg similar in these two widely separated gulfs of L. Victoria concentrations compared with temperate piscivorous fish. which had different water qualities and anthropogenic The water Hg concentrations were similar in Napoleon impacts, demonstrating that food web studies in one gulf (Uganda) and Winam (Kenya) Gulfs, but the THg may be extrapolated to another. The freshwater shrimp concentrations in their biota were significantly different, Caridina nilotica, now present in nearly all habitats and which may have been due to biogeochemical differences eaten by most fish species, had a wide range of C values in the two gulfs. Concentrations of THg in Nile perch but low N values. and Nile tilapia increased with total length of the fish in Studies of pelagic biological nitrogen fixation in both gulfs at the same rate of increase. The rates of THg inshore and offshore waters of northern Lake Victoria bioaccumulation for each food web were within the showed that it was high (often more than 0.5 μg N per range of those observed in temperate and tropical lakes litre per hour), greatly exceeding estimates of atmospheric elsewhere, suggesting that (as in L. Malawi) Hg nitrogen and river input (Mugidde et al., 2003). accumulates at a similar rate in diverse food webs N-fixation increased with light availability and maximal regardless of latitude and species composition. In the rates occurred when the lake was thermally stratified and Jinja area of L. Victoria, Ramlal et al. (2003) found mercury mixing limited to a shallow layer at the surface. Algal in muscle tissue of 2+ and 3+ year old Nile perch to be biomass and N-fixation rates were lowest in July when 90–250 ng/g wet weight. Here the average total mercury the lake was mixing more deeply. Nitrogen enrichment in the water column was 7.5 ng Hg L-1, and the average experiments demonstrated that phytoplankton was concentration in the solid top 10 cm of sediments was primarily limited during the early-stratification season; 220 ng Hg g-1 (close to that found in the Laurentian increased light levels resulted in N-deficiency but Fe Great Lakes). Methylmercury in surface water near a additions stimulated N uptake (Guildford et al., 2003). variety of wetland vegetation was low, with the possible Little is known about the concentrations of mercury exception of water collected near roots of water hyacinth (Hg) and factors affecting this contaminant in tropical (Eichhornia crassipes). Although mercury levels in the waters. Bootsma et al. (2003) includes three studies of fish are within the accepted guidelines of the FAO (Food mercury pollution and its transfer through the food and Agriculture Organization of the United Nations) webs: one from Lake Malawi, followed by two from Lake and the World Health Organization, they advised that Victoria. In L. Malawi in 1996 and 1997, Kidd et al. (2003) monitoring of fish mercury levels should be continued found that concentrations of Hg in fish and invertebrates as the diet of the riparian peoples contains so much fish. were generally low (2 to 200 ng/g wet weight). The concentrations were considerably higher in pelagic fish

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 138 Lowe-McConnell, R.

Lake Tanganyika fisheries pelagic fish catches, but concluded that, although surface temperatures do indeed show warming trends, evidence The deepest lake in the Rift Valley, Lake Tanganyika, for decreased productivity is ambiguous and no overall has a remarkably rich cichlid fauna at the generic level, decline in fish catches has been documented. Total lake- attributable to the steep rocky shores which shelter the wide catches increased up to 1995 as regional declines cichlid communities from four endemic species of Lates in the industrial fishery have been compensated for by and many other predators. The main commercial fishery lake-wide increases in artisanal catches. Since the present was an open water ring-net fishery for pelagic clupeids. evidence is not sufficient to demonstrate the effects of Burundi has provided one of the longest records of climate change on fish stocks, this suggests intensification catch statistics (1956–1992) for any tropical fishery, and of the fishery has been the major factor in these changes. these were analysed by van Zweiten et al. (2002). More Plisnier et al. (2009) have examined fluctuations in recently, data on wind patterns, evaporation and physical abundance of the clupeid Stolothrissa tanganicae and of variables affecting the L. Tanganyika fisheries have been the pelagic Lates stappersii and found that these species collected from several automatic sampling stations and now fluctuate on considerably different time scales, with meterological buoys on the lake. These have shown that an inverse correlation between their abundances, which nocturnal mixing in the south is more dependent on wind had previously been attributed to the consequence of forcing and evaporation, while heat loss from the surface predator–prey relationships. Currently, however, the two plays a more important role at the north end of the lake species appear spatially segregated in the lake, S. tanganicae (Verberg & Hecky, 2003). External nutrient sources for the dominating in the north while L. stappersii is generally more lake, assessed from the physico-chemical characteristics abundant in the south, where it feeds mostly on shrimps, of the three largest inflowing rivers (Rusizi, Malagarasi not clupeids. The limnological factors associated with and Lufubu), showed that the Rusizi provided the most variability of these fish catches indicated that abundance and Lufubu the least of total riverine nutrient inputs. Wet of S. tanganicae was positively correlated with plankton atmospheric deposition (rainfall) provided approximately biomass, while for L. stappersii water transparency, depth 83 % of dissolved inorganic nitrogen, 37 % of total of mixed layer and oxygenated water appeared to be the phosphorus, 63 % of total dissolved phosphorus and 64 % important drivers of its abundance. Alternating mixing of soluble reactive phosphorus, but only 1 % of soluble and stable states of the epilimnion, related to seasonal and reactive silicate, the remaining load being derived from internal wave variability, probably determine the short-term riverine sources. External loading forms the main pathway variability in abundance of both species. There was a close for nutrients to enter the productive layers of the lake relationship between phytoplankton blooms at the time of during stratified periods (February to May) (Langenberg trade wind changes and increased catches of S. tanganicae in et al., 2003). the south. The ‘anti-correlated’, alternating abundances of Langenberg (2008), in a series of papers with full S. tanganicae and L. stappersii probably reflect the underlying bibliographies written for his PhD on the limnology of fluctuations of the limnological environment, clearly Lake Tanganyika, gives data on the limnological annual showing that fisheries studies need to integrate limnological cycle inferred from physico-chemical fluctuations, and planktonic monitoring in order to understand large wind induced changes in the plankton community, and complex ecosystems such as Lake Tanganyika. carbon flows and trophic structure in the pelagic food McIntyre et al. (2006), who studied the effects of nutrient web, and whether climate change has had an impact availability and grazers in the littoral zone of L. Tanganyika on productivity. He questioned whether increases in near Kigoma during the dry seasons of 2001 and 2002, regional temperatures, related to global climate change, found that fish and other large grazers had much stronger had resulted in a substantial decline in L. Tanganyika’s effects on periphyton than did the nutrients, concluding

© Freshwater Biological Association 2009 DOI: 10.1608/FRJ-2.2.2 Fisheries and cichlid evolution in the African Great Lakes 139 that littoral nutrient availability did influence periphyton The clear warm waters of lakes Malawi and Tanganyika productivity but top-down control predominated. also attract aquarists, which has led to many colourful Deep-drilled cores from Lake Tanganyika have been publications (for example Brichard, 1978; Konings, 1995; used by Tierney et al. (2008) to reconstruct precipitation and other Tropical Fish Hobbyist publications). In the and temperature variations during the last 60 000 years. more turbid (and with a risk of bilharzia infection) waters These cores showed that temperatures in L. Tanganyika of L. Victoria, SCUBA was only used later, in clear water follow Northern Hemisphere insolation. They indicated around rocky islands at the south end of the lake, by HEST that warming in SE Africa during the Last Glacial teams from Leiden University. Here they discovered Termination began to increase ca. 3000 years before a whole new community of cichlids (locally known as atmospheric carbon dioxide concentrations started to mbipi), comparable with the mbuna rock cichlids of L. increase. Hydrogen isotope data from two deep sediment Malawi (Seehausen, 1996). cores also showed that this region experienced changes in hydrology at the same time as orbital and millennial events Lake Malawi cichlids in the Northern Hemisphere monsoonal climate records. This implies that precipitation in tropical SE Africa is more Historically, sediments in deep cores and seismic records strongly controlled by changes in Indian Ocean surface have shown that extremely arid conditions existed in temperatures than by the migration of the Intertropical tropical Africa in several discrete episodes, resulting in Convergence Zone. These influences from outside the very low lake levels between 135 000 and 90 000 years lake system on rainfall in the Tanganyika basin help to ago. From well-dated paleoecological records Cohen et al. explain the variance in pelagic fish catches found when (2007) found that Lake Malawi (currently 706 m deep), was the very long series of catch records from L. Tanganika reduced to a ca.125 m deep, saline, alkaline, well mixed pelagic fisheries was analysed by van Zweiten et al. (2002). lake until aridity diminished after 95 000 years ago. Lake levels then rose erratically and salinity/alkalinity declined, Cichlid evolution reaching near modern conditions after 60 000 years, i.e. approximately 30 000 years ago. This record of lake levels The classic taxonomic investigations of cichlid species flocks and changing limnological conditions has provided a in the African Great Lakes were based on collections at the framework for interpreting the evolution of L. Malawi’s British Museum Natural History (now the Natural History fish and invertebrate species flocks. More than 500 species Museum) (see Bertram et al., 1942 and Trewavas, 1983 for of cichlid fish have evolved in L. Malawi within the last Lake Malawi; Greenwood, 1974 for Lake Victoria), and at million years, from only a few common ancestors. Their Tervuren in Belgium (see Poll, 1956 for Lake Tanganyika rapid diversification has been attributed to morphological cichlids). When stationed at Nkata Bay on L. Malawi, adaptation to use very diverse food sources, and to sexual Fryer (1959) described the cichlid communities adapted selection. for life either on rocky or sandy shores, before the advent Establishing relationships among these taxa using of SCUBA permitted underwater observations of these molecular methods had been frustrated by the persistence communities by Ribbink and teams from the JLB Smith of ancestral polymorphism within species. Albertson et Institute, Grahamstown, South Africa (Ribbink et al., 1983; al. (1999), however, averaged the evolutionary history Lowe-McConnell, 1987). In L. Tanganyika, the ecology and of thousands of genes among closely related Mbuna behaviour of cichlids inhabiting rocky shores were studied cichlids, to produce a dendrogram indicating that over 20 years by teams of Japanese and African scientists adaptive divergence in trophic morphology played an organised by Prof. H. Kawanabe, of Kyoto University, important role during the early history of the lake, but Japan (see Kawanabe et al., 1997; Lowe-McConnell, 2003). subsequent species diversity has arisen with little change

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 140 Lowe-McConnell, R. in trophic morphology. This suggested that other forces to reduced predation pressure by Nile perch but also to are responsible for the continued speciation of these fishes. increasing eutrophication, leading to reduced oxygen in Later, Albertson (2008) studied jaw morphology as a the water (hypoxia) and loss of water clarity, which is so predictor of feeding performance and habitat partitioning important for breeding success in cichlids whose sexual in six species of the rock-dwelling Tropheops species behaviour is visually-orientated. complex in L. Malawi. The conclusion was that, for these In addition to studying ecological changes in the lake, species, depth was a major axis of trophic niche partitioning morphological and genetic changes in the species that within this complex, and competition for trophic resources recovered have been made by comparisons with material (epilithic organisms) had led to habitat partitioning and the from HEST’s earlier collections, housed at Naturalis establishment and maintenance of the Tropheops species. (National Museum of Natural History) in Leiden, where George Turner and his team, now based at Bangor more than 120 000 specimens of over 400 species from University, UK, have continued studying sexual selection in Lake Victoria are stored and information is now available Lake Malawi cichlids. Their numerous recent publications on a computerised catalogue. The recovering species include, for example, Genner et al. (1999) and Genner & revealed changes in habitat, an increase in fecundity and, Turner (2005) in which the mbuna cichlids of L. Malawi most strikingly, changes in diet. Both zooplanktivores and are used as a model for rapid speciation and adaptive detritivores had switched to macro-invertebrates (as had radiation. Barson et al. (2007) reported on the genetic some non-cichlid species). Least affected have been the architecture of colour differences between L. Malawi rocky shore species living where they are protected from cichlid species, while Genner et al. (2007a) have found Nile perch predation. There has been a differential impact reproductive isolation among deep water cichlid fishes of on different trophic groups: large species like piscivores, L. Malawi differing in monochromatic male breeding dress. molluscivores and insectivores declined faster than zooplanktivores and detritivores, and the latter now had Cichlid speciation in Lake Victoria many suspected hybrids. Was this because detritivores spawn in more turbid areas? By 2001, the zooplanktivores The haplochromine species flocks in Lake Victoria are had reached their previous level of abundance but their among the most striking examples of rapid evolution diversity had declined from more than 12 species to only known; ecologically they are as diverse as those that three. Although four detritivorous species reappeared, have evolved in the older lakes Malawi and Tanganyika. they made up only 15 % of the number of individuals, Trophic specialisation is the basis of their radiations in while zooplanktivores made up more than 80 %. Currently, L. Victoria and they have evolved into at least 16 trophic zooplanktivore densities are higher than before the ecological groups, with body form and teeth specialised for life such changes, whereas those of detritivores are much lower. as detritivores, zooplanktivores, insectivores, prawn-eaters, When reconsidering these changes in cichlid diversity molluscivores or piscivores (of which there are more than and the reputedly ‘1ost’ species, the HEST team found that 100 species). The HEST team from Leiden University has haplochromine abundance has increased since the decline been monitoring these cichlids from their field station near of the Nile perch in the late 1990s but the number of species Mwanza for nearly thirty years. As populations of the is lower and the trophic composition has changed. A few introduced, predatory Nile perch have diminished, the of the ‘lost’ species have been rediscovered in different main excitement has been the reappearance of about 20 of areas, but the sampling of many habitats during the the 200 ‘lost’ haplochromine species, previously thought past 18 years has yielded only a few of the 200 or more to be possibly extinct. The Leiden team had a unique species they estimated as being lost. The group’s work opportunity to investigate how the resurgent species have on these haplochromines has been summarised by Witte adapted to the changed ecological conditions, not only et al. (2007a, b), each paper having a good bibliography.

Ecological adaptations in the recovering zooplanktivores cones and increased size of the red/green sensitive double have included increased fecundity, habitat extension and cones. How have Lake Victoria’s haplochromine species shifts to a more generalised diet, including larger and less flocks evolved faster than any other known vertebrates? evasive prey that can be obtained without good visibility. Witte and colleagues, who looked at morphological Trophic groups like prawn-eaters and parasite eaters were changes in H. pyrrhocephalus, described how gill surface absent, piscivores were rare and only a few large mollusc- had increased by 64 % enhancing oxygen uptake. Head crushing specimens were seen. The new data suggest length and head volume had decreased in size, which may that although Nile perch predation strongly reduced enhance their ability to accelerate in sudden bursts to escape haplochromine densities in general, eutrophication, Nile perch (Chapman et al., 2008). Eye length also decreased rather than Nile perch predation, has reduced the which may have created a space for larger gills. Small eyes species diversity, possibly by hybridisation and selective generally reduce resolution. So this could be responsible eradication of species that need clear, oxygen-rich water. for the larger prey types in their diet. A marked increase To find out how closely related species had responded in the depth of muscle responsible for the biting force of to environmental changes, the HEST team chose a pair of the pharyngeal jaws is probably a response to the changed species (Haplochromis heusinkveldi and H. pyrrhocephalus) diet. These striking morphological changes had been made which formerly had almost identical distribution and over a time span of only two decades. Is it the combined migration patterns and were equally abundant before the results of phenotypic plasticity and genetic changes which Nile perch boom. Why then had H. heusinkveldi vanished have helped the recovery of this species (Witte et al., 2008)? while H. pyrrhocephalus became the commonest species in Chapman et al. (2008) tabulated studies providing Mwanza Gulf? The team found differences in: a) the retinal evidence for phenotypic, morphological and diet structure of their eyes – H. pyrrhocephalus had eyes better changes coincident with the Nile perch introduction adapted to low-light conditions allowing it to breed under in these haplochromines and other species in Lake lower light conditions than H. heusinkveldi; b) ecological Victoria. These include gill size in the mormyrids differences in their diets – H. heusinkveldi used to include Gnathonemus victoriae and Petrocephalus catastoma, phytoplankton in its diet; and c) in their spawning times changes in gills, body shape and diet in Rastrineobola – H. heusinkveldi had a spawning period limited to months argentea, and diet in Oreochromis niloticus, Lates niloticus with high water transparency whereas H. pyrrhocephalus and the catfishes Bagrus docmak and Schilbe intermedius. is less restricted. In another recovering zooplanktivore The investigations of diet shifts, made by comparing (H. tanaos), formerly restricted to shallow sandy bottoms stomach contents of small benthivorous cichlids caught but now found over mud, the eyes had adapted to the before and after the ecological changes, showed that the lower water clarity by a shift in retinal structure allowing diet of these species had shifted from one dominated by better usage of ambient light of longer wave lengths detritus and phytoplankton (supplemented by small (Witte et al., 2005). Analysis of Nile perch stomachs quantities of midge larvae and zooplankton) to a diet of since 2005 showed that small Nile perch were once again larger-sized invertebrate prey. These species now had feeding mainly on small haplochromines, whereas at the a more carnivorous diet, and concomitantly the ratio of beginning of the1990s they were eating mainly shrimps, intestine length to fish length had decreased by 30 %. The Rastrineobola and juvenile Nile perch (Katunzi et al., 2006). stomach contents of the former detritivores, which now When compared with HEST’s earlier material, some have a diet very similar to that of the zooplanktivores, species revealed morphological changes which seemed contained midge larvae, shrimps, molluscs and a very adaptive to the new environmental conditions, including small amount of detritus and phytoplankton (Kishe- increased gill area, changes in the feeding apparatus and Machumu et al., 2008). Wanink had also found changes changes to the eye retina, with a loss of blue-sensitive single in gill structure and diet in the zooplantivorous pelagic

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 142 Lowe-McConnell, R. cyprinid Rastrineobola in these same waters. The multiple mate choice which could exert diversifying (disruptive) strategies used by Lake Victoria cichlids to cope with life- sexual selection causing rapid speciation in these cichlids. long hypoxia have been examined by Rutjes et al. (2007) Seehausen (now at University of Bern and Eawag who concluded that lifelong adaptation is mainly due to (Swiss Federal Institute for Aquatic Science)) and 12 co- improved oxygen transport within the blood system. authors, in ground-breaking work combining many Eutrophication has also led to much reduced techniques (Seehausen et al., 2008), have now demonstrated penetration of light into Lake Victoria. This has sensory-driven speciation within island populations of influenced the strategies of the cichlids for foraging and cichlid fish by identifying the ecological and molecular for communication, including the visual signals used for basis of divergent evolution in the cichlid visual system. mate choice, as shown by HEST in an earlier study by They have also demonstrated associated divergence in Seehausen et al. (1997). The wave length of downward male colouration and female preferences, and shown transmission of light into water depends on the content subsequent differentiation at neutral loci indicating of dissolved and dispersed organic materials. In clear reproductive isolation. The evidence was replicated lakes (and oceans) light becomes bluer as path length in several pairs of sympatric populations and species. increases while, in water carrying green organic matter, Variations in the slopes of the environmental gradients light becomes greener and, with undecomposed products explained variation in progress towards speciation, which of plant and animal decay, light shifts to longer (red) wave occurred on all but the steepest gradients. Thus they lengths. Seehausen et al. (2003a) discussed the theoretical have provided the most complete demonstration so far effects of visual range on foraging, niche partitioning, and of speciation through sensory drive without geographical coexistence with predators; and the effects of colour vision isolation. Their results also provide a mechanistic on cichlid foraging, communication and coexistence. They explanation for the collapse of cichlid fish species diversity concluded that increased turbidity caused by increased during the anthropogenic eutrophication of L. Victoria. eutrophication (possibly in combination with the effect of A masterly summary in graphical form puts together visual range on selectivity of mate choice) might explain data on ecological, phenotypic, genetic and behavioural the rapid erosion of cichlid species richness in L. Victoria differentiation between blue and red Pundamilia nuptial in recent years. Using a transect of littoral research stations phenotypes at five islands. This shows how adaptation of a in the clear water off small rocky islands in southern haplochromine’s eyes and colours to its visual environment L. Victoria, they found that the number of coexisting has biased cichlid females to mate with different males cichlid species was positively correlated with the width according to their colouration, a preference which can of the light band. Furthermore, along this transect the contribute to the formation of new species sympatrically. proportion of putative hybrids between two sympatric They have shown this by working with two species species (Pundamilia pundamilia and P. nyererei) was inversely (‘blue male’ Pundamilia pundamilia and ‘red male’ P. correlated with light band width; and off very turbid or nyererei) which typically have blue or red male spawning very steep shores, which had a very narrow light spectrum, colours respectively. These males were found to have a each haplochromine genus was represented by just one genetic variation for visual sensitivity to these colours; in species, whereas there were up to six species per genus at some populations females with blue-biased vision seem locations with broad light spectra (Seehausen et al., 1997). to mate only with blue males, red-biased females only Associated breeding experiments in aquaria showed with red males. The authors therefore suggested that that with haplochromines exhibiting different coloured barriers could arise within a population, so it does not, as breeding males, females vary in their preferences for mates some had previously thought, require a phase in which of different colour variants, demonstrating a potential for red and blue populations have evolved allopatrically. Lake Victoria has diverse visual environments; in turbid

© Freshwater Biological Association 2009 DOI: 10.1608/FRJ-2.2.2 Fisheries and cichlid evolution in the African Great Lakes 143 water and on steep sites this spectral shift is rapid, on therefore, may be an important agent of diversification gently sloping beaches more gradual. Starting from the previously neglected among studies of cichlid fishes. shore and descending along the bottom, red becomes The females of all these haplochromines are mouth increasingly dominant in the visual spectrum. To find brooders in which the female broods eggs in her out what the fish see, the team identified genetic variables mouth then guards the young after they hatch. Using (alleles) in one of the opsin genes in eye tissue responsible P. pundamilia and P. nyererei (caught from Mkobe Island) for tuning the fish’s sensitivity to different colours. Then, in cross-fostering experiments, Verzijden & ten Cate by cultivating eye tissue genes in vitro, and measuring the (2007) obtained evidence that learning in the form of absorption properties of the resultant proteins, they found sexual imprinting helps to maintain reproductive isolation some variants red biased in their sensitivities, others blue among closely related cichlid species. By swapping eggs biased. In the lake the numbers of males with red, blue or between the mouths of red and blue morph mothers intermediate nuptial colours varied between populations. they found that female fish raised by foster mothers At Mkobe Island, where the spectral shift was neither belonging to a different species from their genetic mothers, very rapid nor very gradual, blue males were confined preferred males of that different species. This suggests to the shallows, red males to greater depths; at this site that learning at a young age contributes to reproductive the blue males carried the blue-biased opsin variant, isolation in these cichlids, in addition to other mechanisms. whereas most red males carried the red-biased variant. Maan et al. (2008), from field observations of the Colour morphs also showed differences in other genetic colour polymorphic Neochromis omnicaeruleus in Lake markers suggesting they are nascent species. At sites Victoria, found that blotched fish incurred more predator where the spectral shift was rapid, intermediate colour attacks from wild birds. Underwater observations forms were found and genetic differentiation was absent. revealed behaviour differences between the sexes which Red and blue colour morphs occur in other cichlids entailed an additional predator risk for males. This (Seehausen & Schluter, 2004) suggesting that colour differential predation with regard to colour pattern polymorphism may be very ancient and the red and and sex may be another important selective force in the blue-biased opsin alleles much older than in the species evolution and maintenance of colour polymorphism. studied here. This led Seehausen et al. (2008) to suggest that one key to the spectacular species radiation of African The origins and evolution of the cichlid lake cichlids may be that they have inherited from distant species flocks ancestors a trove of genetic variation for sensory systems and male signals, possibly contributed during an inferred Where did these cichlid species flocks originate? In an episode of interbreeding 20 000 years ago, and this important paper, nine authors collated information on the variation may be entrained again and again in speciation origins of the Lake Victoria and Lake Malawi species flocks events. Using a large dataset of the distributions and from riverine haplochromines, using information based nuptial colours of 52 cichlid species on 47 habitat islands on phylogenetic analyses of polymorphism in nuclear in Lake Victoria, Seehausen & Schluter (2004) tested DNA (Seehausen et al., 2003b) which they contrasted with their hypothesis that competition between males for mitochondrial DNA data published previously (Meyer et breeding sites promotes such colour diversification and, al., 1996). The later analyses suggested that the species flock thereby, speciation. The distribution of closely related of the L. Victoria region is derived from a single ancestral species over the habitat islands was determined by species found in the rivers of East Africa and closely related nuptial colouration and implied that selection of nuptial to the ancestor of the L. Malawi flock. The L. Victoria flock colouration is a sufficiently strong force to override other contains ten times less mt DNA variation than the L. Malawi effects of species distributions. Male to male competition, flock. This is consistent with the current ages of the lakes,

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 144 Lowe-McConnell, R. for which molecular and geological evidence agrees that The nuclear genetic data did not confirm strict colonisation in L. Malawi occurred between 500 000 and monophyly of either the Victoria or Malawi species flocks 2 million years ago, whereas geological and palaeolimno- but raised the possibility that these flocks have arisen from logical evidence has indicated that the L. Victoria basin is hybrid swarms (Seehausen, 2004). The species flocks in lakes ca. 400 000 years old, although the lake was dry for several Victoria and Malawi have, it seems, evolved independently thousand years and only refilled about 15 000 years ago. and hence the extensive parallelisms in morphology In a review of geophysical and paleoecological evidence and evolution in some of their cichlid species probably Stager & Johnson (2008) state that L. Victoria was at its reflect true parallelism, similar to that shown between lowest level between 14 000 and 18 000 years ago and cichlid species endemic to lakes Tanganyika and Malawi. dried out at least once during that time. They found no How old are the cichlid radiations in the African evidence of remnant ponds or marshes and concluded Great Lakes? New dates for the lake radiations are given that L. Victoria’s diverse biota must be reconciled with the by Genner et al. (2007b) who report that phylogenetic incontrovertible geophysical and paleoecological evidence reconstructions are consistent with cichlid origins prior of the ca.15 000 year age of this lake. to Gondwana landmass fragmentation 121–165 million Low genetic variation in the Lake Victoria flock had years ago, considerably earlier than the first known cichlid made it hard to understand how selection could have fossils (Eocene). They found that accumulations of genetic produced the large functional diversity observed in a time diversity within the radiating lineages of lakes Malawi, that translated into between 30 000 cichlid generations Victoria, Barombi Mbo, and the Palaeolake Makgadikgadi, for L. Victoria and 400 000 for the entire Victoria–Edward began around, or after the time of, basin formation. region. The nuclear markers used in the study by Seehausen Calibrations suggest Lake Tanganyika was colonised et al. (2003b), however, now showed unexpected genetic independently by the major radiating cichlid tribes that variation and a Congolese–Nilotic origin of the L. Victoria thereafter began to accumulate genetic diversity (contrasting cichlid species flock; it demonstrated that the Victoria– with the widely accepted theory that diversification Edward flock is derived from the morphologically and into major lineages took place within the L. Tanganyika ecologically diverse cichlid genus Thoracochromis from the basin). Their evidence suggests that ancient lake habitats Congo and the Nile, rather than from the phenotypically have played a key role in generating and maintaining conservative East African Astatotilapia (as formerly diversity within radiating lineages, also that the lakes believed). This result is not entirely surprising as rivers have captured pre-existing cichlid diversity from multiple feeding L. Victoria were tributaries of the Congo until the sources from which adaptive radiations have evolved. region west of the lake became elevated ca. 400 000 years ago Lake Tanganyika contains the highest diversity of and they subsequently became tributaries of the Nile. This ancient cichlid lineages. Its basin is believed to have started finding also implied that the ability to express much of the to form around 20 million years ago, initially as extensive morphological diversity found in the flock may far predate swampland, attaining deep-lake conditions some 6–12 the origin of the lake. As the new data indicate, the nuclear million years ago. Dates indicate ancestors of every major diversity of the Victoria–Edward species flock is similar to tribe entered the lake independently and that molecular that of the Lake Malawi flock. This also indicates that its diversity within some tribes began to accumulate around genetic diversity is considerably older than the 15 000 years the time of colonisation, or in two cases (Trematocarini and since L. Victoria began to refill and, in the L. Victoria cichlid Ectodini) possibly before colonisation. The Haplochromini species, most of the variation was manifested in trans- may have split into several lineages prior to the formation species polymorphisms which also suggests very recent of deep-water conditions. At least two haplochromine cladogenesis from a genetically very diverse founder stock. lineages colonised the basin independently prior to rifting. The first lineage, Pseudocrenilabrus, has one

© Freshwater Biological Association 2009 DOI: 10.1608/FRJ-2.2.2 Fisheries and cichlid evolution in the African Great Lakes 145 species in the catchment, the second contains Tropheini, rates of speciation, whereas ca. 0.5 million years into a a group endemic to the lake basin that has radiated into radiation speciation becomes much less frequent. The a large number of species/geographical races. The genus numbers of species in a radiation increases with lake size, Astatotilapia includes A. burtoni from an East African supporting the prediction that species diversity increases haplochromine mt DNA lineage and A. stappersii of the with habitat heterogeneity, also with the opportunity for Lake Victoria-region lineage, and may also be related isolation by distance. Finally, the propensity to radiate to some Lake Malawi species (Seehausen et al., 2003b). within lakes is a derived property that evolved during Within the Lake Malawi haplochromine radiation, the evolutionary history of some African cichlids and comprising 450–600 species in around 50 genera, the onset does not coincide with the appearance of proposed of accumulation of genetic diversity was dated to 4.63 key innovations in cichlid morphology and life history. and 2.44 million years ago, estimates which support the The cichlid fish of Lake Tanganyika also present a hypothesis that the flock radiated within the timescale of celebrated example of species diversification with a rich the basin’s history. The rifting that formed L. Malawi is literature. As population subdivision is likely to play an now estimated to have begun 8.6 million years ago, with important role, Wagner & McCune (2009) contrasted deep-water conditions attained by 4.4 million years ago. patterns of spatial structure in sympatric cichlid species The age of the Lake Victoria region cichlid fishes is living in a mosaic of rocky and sandy habitats north of more controversial. Over 600 closely related cichlid species Kigoma, to find out how habitat features interact with comprise the East African ‘superflock’ inhabiting lakes demographic, behavioural and ecological attributes to Victoria, Kyoga, Rukwa, Kivu, Albert, George–Edward and influence gene flow and population divergence. Using surrounding water bodies. Within this superflock region, multilocus microsatellite genotypes they contrasted L. Victoria forms a phylogenetic zone largely distinct in population differentiation in two species of Petrochromis mt DNA from the western rift lakes Albert, George–Edward and a Simochromis species and found that, despite their and Kivu. Divergence within the L. Victoria catchment close phylogenetic relationship and shared habitat affinity, has been dated to between 120 000 and 89 000 years ago, they showed striking differences in their patterns of estimates that suggest diversity arose after the formation of genetic subdivision within the same geographical region, the L. Victoria catchment approximately 400 000 years ago. indicating different patterns of gene flow. In particular, the Seehausen (2006) reviewed the literature and identified two trophically specialised Petrochromis species exhibited a 33 intralacustrine radiations and 76 failed radiations much more restricted gene flow over sandy habitat than which he then related to lake size, age, and phylogenetic did the trophically opportunistic Simochromis species. This relationships of the cichlids. In doing this, he addressed shows how ecological and behaviour traits have a strong two questions: (i) whether the rate of speciation and influence on the scale and degree of population subdivision. resulting species richness are related to temporal and The ecological causes of evolutionary diversification spatial variation in ecological opportunity (a key prediction are a major focus of biology but little has been said about of ecological theory but untested for cichlid radiations), the effects of evolutionary diversity on ecosystems. and (ii) whether the likelihood of undergoing adaptive Studying the three-spined stickleback (Gasterosteus radiations is similar for different African cichlid lineages aculeatus), Harmon et al. (2009) have shown that adaptive (as suggested in a former hypothesis that the propensity of radiations, even over short timescales, can have profound cichlids to radiate is due to a key evolutionary innovation effects on ecosystems. This stickleback has, within the shared by all African cichlids). He found evidence past 10 000 years, undergone parallel diversification in suggesting that speciation rate declines as niches get several lakes in coastal British Columbia, resulting in the filled during adaptive radiations: young radiations and formation of two specialised species (benthic and limnetic) early stages of old radiations are characterised by high from a generalised ancestor. Using mesocosm experiments

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151 146 Lowe-McConnell, R.

Harmon et al. have demonstrated that this diversification unintentional experiment on a vast scale), whereas many has strong effects on ecosystems, affecting prey community cichlid species living on open sandy/muddy bottoms, structure, total primary production and the nature of where they lacked cover, vanished during the Nile perch dissolved organic materials that regulate the spectral boom. properties of light transmission in the system. These Forty years ago studies on the sympatric tilapia effects all reflect the complex and indirect consequences of species in Lake Nyasa (Malawi) where they are most ecosystem engineering by sticklebacks. When commenting readily distinguished by male nuptial colours, strongly on this paper, Seehausen (2009) has stressed how their suggested some form of sympatric speciation must be evidence that speciation and adaptive radiation can change involved. The idea of sympatric (as opposed to allopatric) the properties of an ecosystem is a reminder of the pressing speciation was then hotly contested (as discussed by need to integrate ecosystem science and evolutionary Lowe-McConnell, 1987, chapter 5) as no mechanism for biology. He adds a warning that, with the rapid human- this had then been determined. So recent demonstrations induced collapse of species diversity in ecosystems of speciation without geographical isolation for Lake dominated by recent adaptive radiations, we should expect Victoria’s haplochromine cichlids, together with news of to see the collapse of nascent species diversity, leading to further studies on other spectacular cichlid species flocks severe perturbations in ecosystem functioning – a process in both lakes Malawi and Tanganyika, is very gratifying. that may already be underway in the African Great Lakes. Research on these African Great Lakes has demonstrated clearly how knowledge of their very complex fish Concluding Remarks communities (especially of cichlid fishes) has depended on knowing what species of fish are present, the ecology Seehausen (2007) discussed how chance, contingency and and behaviour of individual species, and the limnological historical determinism jointly determine the rate of adaptive conditions governing their life cycles. Lake Victoria, the radiation, pointing out that the two major phylogenetic largest tropical lake in the world is now suffering from severe lineages responsible for most of the adaptive radiations of eutrophication and the probable loss of up to half of its 500+ cichlid fishes in African lakes – the three genera of tilapiines species of endemic cichlid fishes. Eutrophication-induced (Tilapia, Oreochromis, Sarotherodon) and the Astatotilapia- loss of deep-water oxygen, which started in the early 1960s, related haplochromines, widely distributed across African may have contributed to the 1980s collapse of indigenous lakes – often occur together but rarely radiate in the same fish stocks by eliminating suitable habitats. The prime lake. This may imply possible suppression between cause of this change has been the rapid and accelerating unrelated cichlid lineages. In this paper he also referred to rise in human populations of all three lake basins. In the the 1960s dispute on the impact of predators on adaptive L. Victoria basin this has grown from 4.6 million people radiation in these cichlids, citing Lowe-McConnell (1993) in 1932 to 27.7 million in 1995, and is predicted to double who summarised this debate. Lowe-McConnell noted to 53 million by the year 2020 (United Nations, 1995: see that in Lake Tanganyika, the four endemic predatory Verschuren et al., 2002). This rapid population growth, Lates species quite probably inhibited speciation among with immigration and improved health conditions, started the openwater-living fishes, but could have promoted it the pattern of large-scale deforestation and conversion to among the rock-dwelling species for whom cover was agriculture. Palaeolimnological data have now established available, by increasing isolation between the various a strong historical connection between land use and algal populations. The discovery by Seehausen (1996) of a flock production in L. Victoria, which indicates that landscape of cichlids inhabiting the rocky shores in Lake Victoria has disturbance, rather than (or combined with) food web supported this idea as these species survived the impact of alteration from introduced species or climate change, the introduced Nile perch Lates (which had provided an is the dominant cause of the ongoing eutrophication

(Verschuren et al., 2002). Further degradation of the References L. Victoria ecosystem can only be countered if land management strategies severely restrict nutrient input into Albertson, R.C. (2008). Morphological divergence predicts habitat the basin. The maintenance of sustainable fisheries in lakes partitioning in a Lake Malawi cichlid species complex. Copeia Malawi and Tanganyika is also contingent on large-scale 2008, 689-698. implementation of improved land-use practices in the Albertson, R.C., Markert, J.A., Danley, P.D. & Kocher, T.D. (1999). lake basins. The continuous degradation of the ecological Phylogeny of a rapidly evolving clade: the cichlid fishes of functions of these lakes and their fisheries is now likely Lake Malawi, East Africa. Proceedings of the National Academy of to have serious long-term consequences and threaten Sciences of USA 96, 5107-5110. social welfare in the countries bordering their shores. Amaras, J.O. (1986). Editorial letter in newspaperThe Standard, 22 The increasing pressure for more food presents fisheries July, Nairobi, Kenya. managers with the task of reconciling the conflicting Balirwa, J.S., Chapman, C.A., Chapman, L.J., Cowx, I.G., Keheb, K., demands of exploitation and conservation of biodiversity Kaufman, L., Lowe-McConnell, R.H., Seehausen, O., Wanink, (as discussed by Balirwa et al., 2003, and in Crisman et al., J.H., Welcomme, R.L. & Witte, F. (2003). Biodiversity and 2003). Chapman et al. (2008) in their Plenary Lecture for the fishery sustainability in the Lake Victoria basin: an unexpected 30th Congress of the International Association of Theoretical marriage? BioScience 53, 703-715. and Applied Limnology (SIL) on ‘Biodiversity conservation Barson, N.J., Knight, M.E. & Turner, G.F. (2007). The genetic in African inland waters: lessons of the Lake Victoria region’, architecture of male colour differences between a sympatric give an excellent summary, with an extensive reference Lake Malawi species pair. Journal of Evolutionary Biology 20, 45- list, of the threats to biodiversity, fishery dynamics and 53. the interaction of multiple stressors on the sustainability Bertram, C.K., Borley, H.J.H. & Trewavas, E. (1942). Report on the of fisheries, biodiversity and the residual fauna. Their Fish and Fisheries of Lake Nyasa. Crown Agents for the Colonies, physiological studies have shown the importance of London. low oxygen conditions in wetlands (as well as rocky Bootsma, H. & Hecky, R.E. (2003). A comparative introduction to shores) in providing barriers to predation by Nile perch. the biology and limnology of the African Great Lakes. Journal of Great Lakes Research 29, Suppl. 2, 3-18. Acknowledgements Bootsma, H.A., Hecky, R.E., Hamblin, P.F. & Muir, D.C.G. (eds) (2003). The African Great Lakes. Journal of Great Lakes Research Numerous former colleagues have contributed to this 29, Suppl. 2. 293 pp. review by fascinating discussions and sending me the Brichard, P. (1978). Cichlids and all the other Fishes of Lake Tanganyika. most recent literature. I would especially like to thank T.F.H. Publications, Inc. Frans Witte, Frits Roest, Ian Cowx, George Turner, Ellinor Campbell, L.M., Hecky, R.E. & Wandera, S.B. (2003a). Stable Michel, Robert Hecky and Gordon Howes; also Pat and isotope analyses of food web structure and fish diet in Napoleon Mary Morris for help in many ways. Mary Morris has given and Winam Gulfs, Lake Victoria. Journal of Great Lakes Research invaluable help with the preparation of the manuscript. I 29, Suppl. 2, 243-257. am very grateful to the Freshwater Biological Association Campbell, L.M., Hecky, R.E., Nyaundi, J., Muggide, R. & Dixon, for publishing it and to the two anonymous reviewers for D.G. (2003b). Distribution and food-web transfer of mercury in very helpful comments and suggestions. Napoleon and Winam Gulfs, Lake Victoria, East Africa. Journal of Great Lakes Research 29, Suppl. 2, 267-282. Chapman, L.J., Chapman, C.A., Kaufman, F., Witte, F. & Balirwa, J. (2008). Biodiversity conservation in African inland waters: lessons of the Lake Victoria region. Verhandlungen

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Author Profile The author prepared for African studies at the Freshwater Biological Association, then directed by Barton Worthington a pioneer in African lake fishery surveys, and with Ethelwynn Trewavas at the British Museum (Natural History) before undertaking a fisheries survey of Lake Nyasa in 1945–47. She was then based in Uganda from 1948–54 on the staff of the East African Fisheries Research Organisation and from 1987 onwards visited these African lakes repeatedly when she was Convenor of the African Lakes Group of the International Limnological Society (SIL).

DOI: 10.1608/FRJ-2.2.2 Freshwater Reviews (2009) 2, pp. 131-151