Cichlid diversity, speciation and systematics: examples from the Great African Lakes

Jos Snoeks, Africa Museum, Ichthyology- Cichlid Research Unit, Leuvensesteenweg 13, B-3080 Ter­ vuren,.Belgium. Tel: (32) 2 769 56 28, Fax: (32) 2 769 56 42(e-mail: [email protected])

ABSTRACT The cichlid faunas of the large East African lakes pro vide many fascina ting research tapies. They are unique because of the large number of species involved and the ir exceptional degree ofendemicity. In addition, certain taxa exhibit a substantial degree of intra~lacustrine endemism. These features al one make the Great African Lakes the largest centers of biodiversity in the vertebrate world. The numbers of cichlid species in these lakes are considered from different angles. A review is given of the data available on the tempo of their speciation, and sorne of the biological implications of its explosive character are discussed. The confusion in the definition of many genera is illustrated and the current methodology of phylogenetic research briefly commented upon. Theresults of the systematic research within the SADC/GEFLake Malawi/NyasaBiodiversity Conservation Project are discussed. It is argued that systematic research on the East African lake cichlids is entering an era of lesser chaos but increasing complexity.

INTRODUCTION The main value of the cichlids of the Great African Grea ter awareness of the scientific and economi­ Lakes is their economie importance as a readily cal value of these fishes has led to the establishment accessible source of protein for the riparian people. In of varioüs recent research projects such as the three addition, these fishes are important to the specialized GEF (Global Environmental Facility) projects on the aquarium trade as one of the more exci ting fish groups larger lakes (Victoria, Tanganyika, Malawi/Nyasa). to be kept and bred by many hobbyists ali over the Though based on sorne common grounds and con­ world. cerns, these three projects each have different empha­ The economie importance of the cichlids by no ses and time schedules. Of these three, the largest way diminishes their enormous scientific value as emphasis on biodiversity research was placed on the ever-stimulating research subjects for systematists, SADC/GEF Lake Malawi/Nyasa Biodiversity Con­ evolutionary biologists, ecologists, ethologists, servation Project, the first core program of which geneticists, morphologists, fisheries biologists, etc. ended in July 1999. While many scientific studies are of direct relevance As senior systematist of this project, I often had to to the economie importance of these fishes and may deal with questions concerning the numbers of (de­ contribute to a better fisheries management, others scribed and undescribed) fish species in the lakes and are more focussed on purely scientific aspects oftheir the speed of their speciation. Also the poor knowledge fascina ting biology. of current cichlid systematics was repeatedly ques­ tioned, often with a certain amount of scepticism. It is indeed hard to explain to non-taxonomists how diffi­ JouRNAL OF AQUARICULTURE AND AQUATIC SciENCES ClcHLm REsEARcu: STATE OF THE ART cult it is to estimate the number of species present in VOLUME IX the lake and to produce simple descriptions and clas­ Page 150 sifications. It is equally difficult to explain that the y .!/~ ,y ,(/ ,,/ ,..(

large, present day taxonomie confusion in the se fishes fish species than any other lake in the world. is not necessaril y the result of po or quali ty research in Taken in an African context, the described Afri­ the past (a truism easily forgotten). Many problems can cichlids constitute about a third of the total are simply due to the inherent difficulty of the re­ number of i ts fresh water fish fau na ( fig.l ). However, search subject or, in simple words, to the fact that given the large numbers of undescribed species, more these fishes look so similar. It is from a certain feeling so in cichlids than in other families, this ratio will of frustration when trying to answer these FAQ's increase considerably when a more detailed inven­ (Frequently Asked Questions) as weil as possible that tory of the lake cichlids becomes available. this manuscript originated. In aU large East African Lakes, except Albert and Turkana, the majority of fishes belong to the family A unique vertebrate fauna Cichlidae (fig. 2). Several hypotheses have been Systematics is essen ti ail y the study of the diversity of forwarded to explain the aberrantly low numbers in life, in this particular case; of the East African cichlids. Lakes Albert and Turkana, but probably the intrinsic Hence, it is a key discipline in understanding the morphological features (Bauplan) of the ancestors unique features of these fishes. were not the major determining feature in this process A first observation is that the speciose nature of (Snoeks, in press). The relative importance of other cichlids in the Great African Lakes is unmatched in intrinsic versus environmental factors (physical, the world of vertebrates (table 1). This is a direct chemical and biological) is still to be determined consequence ofthe explosive speciation within these (Fryer, 1965;Fryerandlles, 1972;Greenwood, 1994; lakes, the results of which complete!y overshadow the Snoeks, in press). classic textbook example of t~e Galapagos finches. While the highest numbers of cichlids are found in The underlying evolutionary processes that have the three larger lakes, the situation is somewhat differ­ resulted in this multitude of species are subject matter ent for the non-cichlids (fig. 3). In view oftheir large for many specialized publications and will not be size, the three largest lakes do not have a dispropor­ discussed here. tionately large non-cichlid component (fig. 3a). How­ A second feature of this unique fauna is that the ever, while the smaller lakes (Turkana, Albert, Ed­ majority of the species are endemie to a lake, i.e. they ward, and Kivu) harbour mo~ethan athird of the non­ iive only in one lake system and nowhere else (see cichlid fauna, they only comprise a smail fraction (6 below). . . %) of the cichlid fauna present in the East African The two main features (species richness and Lakes (fig. 3b). endem1sm) àlone make the Great African Lakes the The aberrant position ofLakes Turkana and Albert largest centres ofbiodiversity in the vertebrate world. also becomes apparent in a species 1area plot (fig. 4 ). While the data for the non-cichlids are situated rela- . . The African cichlids: the view of the accountant tively close to the fitted linear flinction, the correla- Cichlids are reported to be the third im;gest f~mily of tion is less in the cichlids, which are iimch more fishes (marine, brackish and freshwater) in the world wi~ely scattered around the fitted line. Removing the (Nelson,J994). However, the figure given byNelson data of Lakes Turkana and Albert resulted in a much is without any doubt an underestimate .. Based on narrower dispersal ofthe cichlid numbers aromid the current estimates (Kullander, 1998;Snoeks, in press), regression line. Further exploration of these data the total number of cichlids might weil be around through speeies/vailable volume plots slightly changed 2,400 species, which would make it the large_st family the .relative position of severallakes, but the aberrant of fishes, and even of vertebrates. position of Lakes Albert and Turkana remained (re­ Although many species occur in South and Middle sults not shown). America [estimated at 550 (Kullander, 199&)1, itis in the East African Lakes that cichlids have speciated in greatest profusion. In fact, the cichlids of these lakes Jou~AL oF AQUARICULTURE AND AQUATIC SciENCES constitute more than 10 % of the extant freshwater CICHLID RESEARCH: STATE OF THE ART fishes of the world and each of the three larger lakes VoLUME IX (Victoria, Tanganyika, Malawi/Nyasa) harbours more Page 151 Others Mormyridae

Cichlidae Cyprinidae

Amphiliidae Mastaeembelidae Clariidae Gobüdae Moohokidae Cyprinodontidae

Figure 1. Relative species richness of the fish families living in the Mrican fresh and brackish waters. Data from Cloffa 1, 2, 4 (Daget etal., 1984, 1986, -1990). Meanwhile the taxonomy of certain groups bas changed. Renee the Cloffa concept of Bagridae now encompasses Bagridae as well as Claroteidae and Austroglanididae. Cyprinodontidae are currently Poeciliidae and Aplocheilidae. ENDEMISM HOW MANY SPECIES? AgeneraltrademarkofthecichlidsintheEastMrican This is not an easy question to answer and in a way a region is their high degree ofendemisni (> 90 % in correct answer is not particularly relevant at the most lakes, fig. 5). Again:, outliers for this feature are moment. What needs to be made clear is that, contrary . Lakes Turkana and Albert; Non-tichlid endemism is to the situation in other vertebnite groups su ch as birds far less, but reaches a level of almost 60 % in Lake or large mammals, we arefar from a complete inven­ Tanganyika. This is most likely related t6 the great tory of the African species of fish. Particularly for the ·age of this lake which is èstimated at between 9 and 12 cichlids, estimates vary considerably, but the oum­ million years, with sorne parts of the present day lake bers put forward have to be interpreted in a historical significantly younger (Cohen et al., 1993). context. A summary of curient estimates is given in As if pure species richness and endemism is riot Table 1. Of the total, less than half are scientifically enough for this fauna to be unique, a high intra­ described. The least known are Lakes Victoria and lacustrine endemism (the restricted distribution of a Malawi of which one third and two fifths of the species within the lake itself) is also observed in cichlids are described respectively. certain groups within the three major lakes, Victoria Even near the beginning of the twenty-first cen­ (e.g. Seehausenetal., 1998), Tanganyika(e.g.Snoeks tury new species-rich cichlid assemblages are still et al., 1994 and literature discussedherein) and Malawi/ being discovered in the East African Lakes. Rela­ Nyasa (e.g. Ribbink et al., 1983; Konings, 1995, tively few rock-dwelling haplochromines were known 1996). from Lake Victoria until more than 100 new species were discovered after intensive surveys of the rocky habitats between 1986 and 1996 (Seehausen et al., 1998). Recently, a sub-flock of more than 40 new JouRNAL OF AQUARICULTURE AND AQuAnc SciENCES deep-water Placidochromis bas been discovered in ÜCHLID RESEARCH: STATE OF THE ART VoLUME IX Page 152 .._;.·

Lake Malawi/Nyasa during a two year survey of the tional sources of information that help us to determine SADC/GEF project (Hanssens, 1999). how fast this speciation may have been (see below). Apart from the description of such new species These conclusions have been copied in almost every assemblages, the increase in the number of described paper that touches on the subject of cichlid speciation, species can be very slow. Often, numbers grow by the but a cri ti cal assessment of its biological implications isolated discovery of one or a few species. However, was rarely included. Snoeks (in press) spoke in terms it is incorrect to assume th at newl y discovered species of 'hard to believe' arguments and 'gut feelings' , are necessarily cryptic species that have escaped the unaware at the time of writing that Fry er ( 1997) had observations of scientists or that they live in poorly attacked part of this argument in a much more elo­ explored or difficult to access areas. For example, of quent style, wh en discussing the discrepancy between Neolamprologusfalcicula (Brichard, 1989) only se ven the biological interpretation of the desiccation of specimens are in collections of international institutes Lake Victoria and the biological evidence available. and museums, three of which even belong to another Therefore, I want to express caution against a too undescribed species (Snoeks, pers. obs.). However, sloganesque representation ofcichlid speciation rates. one species, closely related to or conspecific with N. A short review of the information available from the falcicula, bas been discovered near Kigoma on the various lakes is given below. Tanzanian shores of Lake Tanganyika and was found to be the most abundant fish species on she1tered sites Lake Nabugabo. A classical example is the situation with stone and shell assemblages on a sandy bottom in Lake Nabugabo, one of the satellite lakes of Lake (Verburg and Bills, in prep.). Also in well-explored Victoria, in which five of the seven haplochromine trawl areas in the southern part ofLakeMalawi/Nyasa species were found to be endemie (Green wood; 1965). new species are discovered within the more abundant Both lakes are separated from each other by a sand bar species (Turner, 1996; Snoeks, pers. obs.), such as dated 4,000 BP. However, these results date back Diplotaxodon limnothrissa Turner, 1994. from a time when Jess was known about the geo­ Thorough revisions of taxa will inevitably be­ graphie variation in Lake Victoria cichlids (reviewed come an increasingly important component of the in Witte et al., 1997). Therefore, itis possible that the taxonomie research on the cichlids in the future. This five Nabugabo species are [possibly 'were' because can result in increasing as weil as decreasing species of extinction by Nile perchpredation?] present in numbers. Such revisions are on the way for severa! Lake Victoria, since the waters at the Lake Victoria Malawian genera and species groups, su ch . as sideofthesandbarhavenotbeenintensivelysampled Diplotaxodon, Rhamphochromis (Turner ~md (Goudswaard, pers. conim.). Robinson, in prep.), Alticorpus, Nimbochromis, Ctenopharynx, the shallow water Lethrinops, the deep­ Lake Kivu. Also Lake Kivu represents an interesting bodied spotted utaka (Copadichromis) and the deep case study, though the data are Jess equivocal. Lake water Placidochromis (Snoeks ( ed.) in prep.). Similar Kivu harbours sorne 15 endemie haplochrornines revisions are on their way for Tanganyihn taxa such (Snoeks, 1994). The lake bas only been isolated from as theNeolamprologus savoryi (Poli, 1949) comp1ex, theancient Lake Edward basin sin ce 14,000 to 11,000 the Telmatochromis temporalis (Boulenger, 1898) year BP through volcanic eruptions that completely complex (Hanssens and Snoeks, in prep.) and blocked the northem outlet (Pouclet, 1978). However, Ophthalmotilapia Pellegrin, 1904 (Hanssens et al., apparent! y a proto Kivu lake existed before the present 1999). day lake was forrned (Haberyan and Hecky, 1987). Henee one might postulate that the current species or TEMPO OF SPECIATION their ancestors could have already been present at that In most publications dealing with the speciation of time, and probably, because of the difference in cichlids in the East African Lakes, the adjective 'explosive' is used to illustrate the remarkable speed JouRNAL OF AQUARICULTURE AND AQUATIC SciENCES of this process. While at first the explosive speciation ÜCHLID REsEARCH: STATE OF THE ART was perceived as fast in view of the recent origin (in VoLUME IX geological terrns) of the lakes, there are now addi- Page 153 Table 1. Indigenous species richness in the East African Lakes. Cichlid species numbers of Lakes Edward, Victoria, Tanganyika and Malawi!Nyasa are estimates. Only species occurring within the actuallake are taken into account; introduced species are excluded. Lake Edward figures include Lake George species. Modified after Snoeks (in press)

cichlids non-cichlids total

Turkana 8 36 44 Albert 11 37 48 Edward 60 21 81 Kivu 16 7 23 ' Victoria 500 45 545 Tanganyika 250 75 325 Malawi/Nyasa 800 47 847

;{b!.; 4

altitude, there may already have been a certain degree elongated more pelagie living species, a paedophage, of geographical isolation between the fishes of the a species with hypertrophied pharyngeal jaws, etc. two lakes. On the other hand, there are reasons to ( see Snoeks, 1994 for more details) in less th an 5,000 suspect th at (part of) the Kivu haplochromines may be years. It is indeed difficult to envisage (it is at least to of a more recent origin than the lake in its present me) how su ch a morphologically diverse fauna could _ form. According to Haberyan and Hecky (1987), have evolved so rapidly. dramatic limnological changes began around 5,000 BP, including extreme hydrothermal events that may Lake Victoria. According to Johnson et al. (1996) havecaused the turnover of the lake and the elimination Lake Victoria dried out during the Late Pleistocene of the plankton community. This must have caused and began to refill about 12,400 14C years ago. This direct or indirect extinctions of the fauna of higher would imply that the major part of the about 500 trophic levels (Haberyan and Hecky, 1987). Thus endemie haplochromines present in the lake have there is a possibility that many of the present-day evolved subsequent to this desiecation. The haplochromine species of Lake Kivu originated no expectation within the biological community that earlier than about 5,000 BP. By virtue of its complete maybe the lake did not completely dry out and that isolation from the rest of the Victoria 1Edward /Kivu sorne small water bodies persisted, acting as refugia super flock at that time, this would imply a for part of the fauna, (Fryer, 1997; Seehausen, 1999) monophyletic origin of a large part of the Kivu was counteracted and it appears that, at presènt, there haplochromines as is suggested by Lippitsch (1997) is no evidence that any deep-water refugia existed at on the basis of lepidological(séale and squamation) the end of the Pleistocene (Scholz et al., 1998; Johnson characters. However, such arecentextinction scenario, et al., inpress). Although the geophysical evidence is if put ihto the proper perspective, would not simply apparently overwhelming, the scenario causes imply the presence of recently evolved, similarly difficulties in its biological interpretation. Quite looking endemie species, but would also infer the in rightly, Fryer (1997) drew attention to two important situ development of very different morphologies, implications that did not get the consideration they such as those displayed by a pisçivorous species, an deserved. First, he pointed to the extra dimension beyond the simple multiplication of species in a short time span. Indeed, while explosive speciation does JOURNAL OF AQUARICULTURE AND AQUATIC SCIENCES ÜCHLID RESEARCH: STATE OF THE ART not necessarily need to be accompanied by substantial VOLUME IX morphological differentiation, it did so in the Lake Page 154 Victoria cichlids, and this radiation was extremely TURKANA ALBERT EDWARD

non-cichlids

cichlids KIVU VICTORIA TANGANYIKA

non-ciehlids

dchlids MALAWI/NYASA

Figure 2. Proportion of cichlid and non-cichlid species numbers in the large East African Lakes (based on data from Snoeks, in press).

rapid as weil. And this scenario, including the 1994)], this does not diminish the value ofhis argument. development ofali the morphological specializations, The current inventory of non-cichlid species endemie Fryer (1997) argues, few would anticipate in such a to Lake Victoria (including the Victoria Nile and shorttime span. A similar argument bas been developed Lake Kyoga) is six or seven. If one includes the above for the Lake Kivu haplochromines. Second, the affluent ri vers and theirendemics, this numberrises to desiccation scenario implies also the rapid speciation 14 to 17 (De Vos, pers. comm.). An example further in seven non-cichlid families of fishes. This, Fryer elaborated by Fry er ( 1997) in this discussion is the argues, bas no parallel in Africa. While sorne of the presence of the endemie catfish genus Xenoclarias in non-cichlid species he lists as endemie, are not so [for Lake Victoria. However, the morphological gap instance Brycinus sadleri (Boulenger, 1906), Gnathonemus longibarbis Hilgendorf, 1888, Synodontis victoriae Boulenger, 1906 and S. JouRNAL oF AQUARICULTURE AND AQUATIC SciENCES ÜCHLID RESEARCH: STATE OF THE ART afrofisheri Hilgendorf, 1888 have now been found in VoLUME IX the Malagarasi Basin as weil (De Vos and Snoeks, Page 155 between this taxon and representatives of the genus of the local people. Equally, no evidence of such Clarias may not be as large as previously assumed dramatic changes in lake levels was found in recent! y (Teugels, pers. comm.). The other endemie genus collected cores from the north basin of the lake mentioned by Fry er ( 1997), Cynopanchax is currently (Johnson, pers. comm. in Nicholson, 1998). Based on considered synonymous with Aplocheilichthys and these data one may conclude that certainly Cynopanchax bukobanus (Ahl, 1924) and is more transgression 1 regression cycles have been very wide spread (Wildekamp, 1995). But on the other instrumental in the explosive speciation of the se rock­ hand, a Barbus species, Barbus profundus Green wood, dwelling mbuna, but there is a possibility that the in 1970 is present in the lake and is only found in the situ speciation of the southern mbuna is less recent deeper waters (Stewart, 1977). Qui te correctly Fryer than assumed and happened earlier, when lake levels ( 1997) questioned the origin of the fishes that started to ri se again after a lake level drop of 100 to recolonized the lake. The basic thought behind this 150m sorne five to ten thousand years aga (Ricketts, question is that, if such a large lake as Victoria did dry 1998). In other words, there appear to be indications out completely, what hope was there then for the that the scenario may be right but the timing wrong. smaUer water bodies in the region to survive and act as refugia? Therefore, colonisation most probàbly The problëm=atf':I"c"g"'e;n"u"s.'W:r-rthî::-'llr-.:e-;;c""o=nc""'e~n'""tr"'a:..:h:-;;n'""g,..,o=n"'th~e · -- --­ musthavegonethroughsecondarycontactwithcoastal · obvious problems of recognising species, one often basins, and, perhaps more likely, with the Lake forgets that at the next leve! up, the generic level, Edward/George basin through the Katanga or with many problems still persist and are even becoming the Malagarasi Basin at its upper reaches in the north. more acute than ev er before. To outsiders, it must However a further elaboration of these arguments is appear as if the whole concept of genera for these ·. outside the scope of this paper. Maybe a molecular cichlids has been swept around at rando:rn during the study involving the cichlids of the Lake Edward/ last two decades. This is certainly far fro:rn true, but George basin :may shed so:rne light on the problem. admittedly the problems are still huge. There is no consensus on the use of generic names Lake Malawi. The :most re:rnarkable example of for the cichlids of the Lake Victoria basin (e.g. speciation cornes from Lake Malawi!Nyasa. Owen et Lippitsch, 1993; Snoeks, 1994; van Oijen 1996; · al. (1990) found evidence in the sou them part of the Seehausen et al., 1998). Undeniably, Greenwood's lake of a drastic fall in lake leve! of at !east 121 rn revision (1979, 1980) had a high phylogenetic con­ foUowed by a subsequent rise between the period tent, but taking into account all underlying theoretical from 1390 to 1860. Based on the presence of cichlid and practical aspects subsequently discussed, the species with a restricted distribution on the rocky final issue appears to be one of where to draw the habitats that were dry during the l()w lake stands, they generic line. In this discussion, one has to keep in prudently conclude that" ... distinctive colourforms, :rnind that neither si:rnple species nu:rnbers nor :rnono­ and even good species, have evolved within the space phyly per se can be a justification for the establish­ of200 years." (Owen et al., 1990, p. 544.) and further ment of a genus. Monophyly in this case can be found suggest that" ... many of the ende:rnic species (sensu at aU hierarchicallevels from just below the fa:rnily Ribbink et al., 1983) have evolved in situ within the level dawn to the lev el of two sister species. last 200 years." (Owen et al., 1990, p. 547). However, The status of several cichlid genera is also being according to Nicholson (1998), it appears that if this questioned for Lake Tanganyika. Here, recent and transgression 1 regression cycle (lake lev el fall and ongoing revisions have indicated the need for a thor­ rise) has taken place, then the interval must have been ough review at the generic level. However, this does considerably shorter. And for such an extreme noti:rnply that:rnorphology-based taxono:rny has failed; phenomenon no evidence is found in the oral traditions the truth is that there was si:rnply no :rnorphology­ based phylogeny available. Many Tanganyikan gen­ era were deli:rnited mainly on similarities of the rep­ JouRNAL oF AQUARICULTURE AND AQUATIC SciENCES resentative species, sharing a few easily accessible ÜCHLID RESEARCH: STATE OF THE ART VoLUME IX characters (PoU, 1986). Contrary to the situation in Page 156 Lakes Victoria and Malawi/Nyasa, a phylogenetic fi/ /~// /·

/ ·

approach had rarely been adopted. One example of diate characters, the definitions of Otopharynx and generic confusion in Lake Tanganyika can be found Copadichromis need to be reviewed (Snoeks, pers. in the tri be Eretmodini. The definitions of what were obs.). thought to be well-delimited species and genera need c. The discovery of severa! new species with to be reviewed. This conclusion resulted from the enlarged pores on the head also rendered it difficult to establishment of a molecular phylogeny based on define the differences between Aulonocara and sequences of certain parts of the mitochondrial DNA Alticorpus (Snoeks and Walapa, 1999). which was in partial conflict with the existing classi­ d. A sub-flock of more than 40 species that was fication (Verheyen et al., 1996; Rüber et al., 1999). It recently discovered in the deeper waters (Hanssens, was found that morphological characters that used to 1999) is bridging the gap between Lethrinops and be important for species and genus recognition may Placidochromis, and it might well be that a new genus have been derived more than once within the tri be. At has to be erected to accommodate these species. this moment, there are sufficient morphological data Placidochromis subocularis (Günther, 1893) appears to confirm the status of sorne of the lineage as new to bridge the gap between the genera Placidochromis species, such as the 'E.cf.A' and 'T.cf.E' lineages andMylochromis and may be better accommodated in (Verheyen et al., 1996; Rüber et al., 1999). However, the latter genus. the presence of other taxa within the molecular trees e. The ge nus Sciaenochromis contained predatory is Jess easy to explain, such as 'S.cf.C' and 'Ti 9', and cichlids with a melanio pattern consisting ofan ob­ certainly the situation at the generic level remains lique series of spots and usually traces of the vertical confused. bar pattern as well (Eccles and Trewavas, 1989). In For Lake Malawi!Ny asa, the classification of the the revision by Konings (1993b), all taxa with an haplochromine generais based on the melanio pattern oblique series ofspots were excluded and placed in and morphological features (Eccles and Trewavas, Mylochromis. However, during the identification of 1989). This has lead to situations in which informa­ the SADC collections, we have found sorne more tiQn from the melanio pattern is in conflict with predatory species, highly siinilar to the currently morphological data. In sorne cases the pattern was described taxa of the genus Sciaenochromis, sorne of judged to be more informative; in others morphologi­ which had clear traces of an oblique melanio pattern. cal information was considered to have a higher Clearly a thorough revision is needed. phylogenetic content. A few examples: a. Species with a characteristic striped or spotted Phylogeny melanio pattern but with a special arcade of outer The classification of the East African cichlids was, lower jaw teeth were not attributed to the typical until a decade ago, largely based on morphology­ genera with similar melanio patterns but to the genera inferred phylogenies and/or plain morphological simi­ Lethrinops 1 Tramitichromis 1 Taeniolethrinops be­ larities. However at present most phylogenetic stud­ cause of their characteristic dentition. However, re­ ies are largely the domain of molecular biology. cent! y it has become evident from genetic analyses Morphology-based phylogenetic studies are rare, a that the deep-water taxa of Lethrinops belong, to­ few recent examples being the lepidological studies gether with sorne other groups, to a lineage clearly ofLippitsch (e.g. 1993, 1997, 1998) and an ongoing separate from the shallow-water species (Hauser et study on the lamprologines (Stiassny, 1997). al., 1999). This observation certainly causes doubt In general, molecular-based phylogeneticresearch upon the value of the special dentition as a distinctive on Lake Tanganyika cichlids has been dominated by character for the three genera. However, on the other the direct sequencing approach of parts of the mito­ hand, a quick check of sorne deep-water taxa revealed chondrial DNA. This has been adopted at the popula­ that sorne of them do not have this characteristic tion and species level, and above. Sorne of the results Lethrinops dentition and hence were in the past incor­ rectly included in Lethrinops (Snoeks, pers. obs). JouRNAL oF AQUARICULTURE AND AQUATIC SciENCES b. The melanio pattern/morphology link also broke CICHLID REsEARCH: STATE oF THE ART down for the genus Copadichromis. Furthermore, VOLUME IX with the discovery of sorne new species with in terme- Page 157 Malawi/Nyasa

Turkana Albert Edward Kivu

Victoria Victoria Non cichlids Cichlids

Figure 3. Share of each lake in the total of (a) the non-cichlid and (b) the cichlid fauna of the Great East African lakes (based on data from Snoeks, in press).

obtained clearly stand in contradiction to existing Victoria system. Basically, the results of molecular classifications such as in Tropheus Boulenger, 1898 studies showed very little mtDNA variation between (Sturmbauer and Meyer, 1992; Konings, 1993a; the taxa and indicated that the flock is probably Snoeks, in press) and in the Eretmodines (Rüber et al., monophyletic (Meyer et al., 1994). - 1999). Othermolecular approaches have been adopted as weil, mostly at the supraspecific level (e.g. The SADC/GEF Lake Malawi/Nyasa Takahashi et al., 1998). biodiversity conservation project On Lake Malawi, the mitochondrial DNA ap­ The SADC/GEF Lake Malawi/Nyasa Biodiversity proach (sequencing and RFLPs) was less successful Conservation Project is a multidisciplinary, lake­ in terms of plain taxonomie output. lt resulted in trees wide program involving the three riparian countries, in which lineage sorting was incomplete and that Malawi, Tanzania and Mozambique. lts main scien­ contained ancient polymorphisms. Renee gene trees tific pillars included limnology and water quality, do not necessarily correspond to species trees in systematics and taxonomy, and ecology and conser­ recenily evolved flocks such as the Lake Malawi/ vation. Its core activities and a subsequent short Nyasa cichlids (Moran and Komfield, 1993; Parker monitoring program have recently ended. Within the and Komfield, 1997). Atpresentmicrosatellite anal y­ project great emphasis was placed on the taxonomy of sis has been adopted at the species as weil as the the fishes. This was unique for an international project, population level (Hauser et al., 1999). One practical but on the other band not surprising, since the lake disadvantage of this approach is the large number of harbours more fish species than any other lake in the specimens needed for these studies (Komfield and world. Parker, 1997). The total number of fish species in Lake Malawi/ Less 'genetic' attention has been paid to the Lake Nyasa can be broken down into two subtotals: the number of described species, at present about 360 (cichlids and non-cichlids), and an estimate of the

JouRNAL OF AQUARICULTURE AND AQUATIC SciENCES number of undescribed species. For both categories, ÜCHLID REsEARCH: STATE OF THE ART Lake Malawi/Nyasa holds the world record; the sec­ VOLUME IX ond being of dubious honour, at least to a taxonomist. Page 158 Malawi/Nyasa 6,5 • Victoria• ~ Tanganyi ] 5,5 • e = = 4,5 Tanganyika Edward 0 ... -··· Malawi/Ny~sa- -- - -· --victoria • urkana .... o- --·· o 0 .. ... -····

2,5 Albert • Turkana Kivu 0 • ~ cicblids l,56,5L----,~,5--~-S~,5---~9,5-~--l0~,5------~l1,5 '---o., non-cicblids log area (km 2)

Figure 4. Plot of species numbers (log) versus area (log) of cichlids and non-cichlids in the East African Lakes. A linear function is fitted to the data (based on data from Snoeks, in press).

The lake-wide sampling program. An integrated database is collection based and in eludes ali re--iden­ taxonomy/ecology biodiversity research program, tified specimens. based on a lake-wide sampling scheme, has been A third database contains a list of valid species. At carried out. This included five soft bottom and four present this is mainly based on the classification of rocky shore croises with the RN Usipa. Sorne eigh­ Eccles and Trewavas (1989) for the non-mbuna and teen soft bottom areas from ali around the lake were updated with recent literature. For the rn buna, the data sampled at various depths either by trawling or by gill in Konings (1995, 1996) have been used as a starting netting, and the catches identified and further analysed. point. Almost 700 species are entered in this database Either slides or video shots were taken from as many that is going to be updated on a regular basis. Indica­ representative specimens as possible. During the rocky tions of possible synonymies have been found during shore croises, 29 sites were sampled and their catches the project' s lifespan. On the other hand, se veral tens ànalysed in a similar way as for the soft bottom­ of new species have been found during the project' s sampling program. In addition, underwater observa­ time. Hence the figure of 800 put forward as an tions by SCUBA, including video footage, weremade estimate for Lake Malawi/Nyasa (Table 1). at most of the sites.

Databases. Several databases have been developed JouRNAL OF AQUARICULTURE AND AQUATIC SciENCES during the project. One is arelational database with 15 ÜCHLID RESEARCH: STATE OF THE ART tables linking all aspects of the data collected during VOLUME IX the lake wide surveys (Snoeks, 1999). A second Page 159 80

60

40

20

0 Turkana Edward Victoria Malawi/Nyasa - cichlids AJbert EJvu Tanganyika El non-cichlids

Figure 5. Percentage of endemism of cichlid and non-cichlid species. Endemism is taken in a rather strict sense, as endemism within the lake itself, including sorne obvious parts ofthe effluent basin (Victoria Nile and Lake Kyoga for Lake Victoria; Upper Sbire and Lake Malombe for Lake Malawi), but excluding the affluent drainage system. Note the relative low endemicity of cichlids in Lakes Turkana and Albert, and the high endemicity ofnon-cichlids in Lake Tanganyika (based on data from Snoeks, in press).

Capacity building. The project holds the niost up to the name was 'unknown' or 'unidentified'). This was date library on the biology of the Lake Malawi!Nyasa merely a training in identification, not in taxonomy. fishes (less rich on fisheries publications) and the The difference is crucial but, in my experience, is largest well-curated reference collection in the re­ often being overlooked by decision-rnakers. gion. A local team of one Ph.D. and one M.Sc. student, two research officers and one technician has Systematics and taxonomy. Sorne results have al­ been trained in various aspect of biodiversity re~ ready been mentioned above. Three other relevant search, taxonomy and curating of fish collections. lt outcomes of the project are briefly discussed here. has to be stressed that training of local scientists in Investigations are currently ongoing on what may taxonorny is a new approach. Previously, most train­ be the first case of a combined polychrornatism and ees (fisheries officers and technicians) were taught to polymorphism in a sand-dwelling cichlid of Lake put a fish in a virtual 'box' with a name on it (even if Malawi/Nyasa, Ctenopharynx nitidus (Trewavas, 1935) (Snoeks and Nyasulu, 1999). Polymorphism is the genetically determined occurrence oftwo or more JoURNAL OF AQUARICULTURE AND AQUATIC SciENCES 'rnorphs' within one and the same species (true poly­ CICIILID REsEARCH: STATE OF THE ART rnorphism sensu Greenwood, 1991 ); polychrornatism VoLUME IX Page 160 is a polymorphisrn of color pattern. The differences between individuals of the morphs are permanent existed when lake levels were sorne 450 - 500 rn rather than due to geographie, seasonal or develop­ lower than the current level. At this moment, it is not mental variation (Snoeks, 1995). The possible dis­ possible to define groupings within the non-mbuna, covery of this polymorphism could fuel the former the species of which can be clustered according to assumption that polymorphism may exp lain the large similar distribution patterns. Within the same number of alleged species in African lakes (Sage and genus, species can be found that have a Selander, 1975; Meyer, 1987). However, just the circumlacustrine distribution as well as others with a opposite might be true. The fact is that after identify- much more restricted distribution. However, as lake­ ing tens of thousands of cichlids and reviewing many wide sarnpling has begun only in the last few years, groups to a certain extent, the C. nitidus case remains we have only started to scratch the surface of this the only potential example found of this phenomenon. issue. Another interesting fin ding is th at sometimes mor- phological variation in closely related species may From chaos to complexity not appear to be of similar magnitude. Two species One would expect the taxonomie problems of the past may be difficult to differentiate in a morphometric to be gradually cleared up now that modem methods anal y sis because the small variation in one species is allow us to analyse large morphometric data sets in 'absorbed' bythelargerinthesecondspecies. Thisis much greater detail than ever before, and that new what may have happened in an analysis in which we approaches bring up many use fui complementary were trying to differentiate between Nimbochromis data. Hence order would prevail. However, in this, we polystigma (Regan, 1922) and Nimbochromis may be too optimistic since the order envisaged may livingstonii (Günther, 1893) (Snoeks and Manuel, well be more complex than generally anticipated. 1999), which are otherwise relatively easy to distin- The reasons for this are manifold: The intrinsic guish. On the other hand, it is not excluded that N. difficulty of studying the taxonomy of the cichlids of polystigma as defined at the moment is polyspecific. the East African lakes. Due to the recent speciation, Based on this experience, I would warn against the one cannot expect the various species to be very uncritical adoption of results from a multivariate data distinct in a large number of easily visible features. A analysis in cichlid taxonomy, without a sound 'bio- similar argument is also of importance at the generic logical' review of the existing information. leveL As in Lake Tanganyika ( e.g. Snoeks et al., 1994), Geographical variation. At this moment, for many a unifyingtheory explaining the distribution pattern groups the limits between intraspecific geographical of cichlids in Lake Malawi/Nyasa cannot be estab- variation (within a species) and interspecific lished yet (if ever). Certain is that the occurrence of differences (between species) are very difficult to restricted distributions (intra-lacustrine endemism) is assess. This is perceived differently by so-called far greater in mbuna than in non-mbuna. [The term taxonomie splitters and lumpers and creates the mbuna is used here referring to the eco-morpholog-i--proble-m-of-where-to-draw-the-line-;-!t-is-ineorreet-to------­ cal group of mainly rock-dwelling species as defined assume that this problem-can--be circumvented by by Ribbink et al. (1983) and Eccles and Trewavas powerful multivariate analyses as even small, but (1989). Although the mbuna defined as such are consistent, geographie differences can be picked up considered to be paraphyletic (Moran et al. 1994), and visualised. Therefore, differences between groups mostly 'mbuna' is still used in the traditional sense. of specimens in these analyses do not necessarily Renee, no monophyly is implied.]. While in Lake point to the existence of different species. Tanganyika the split in three subbasins can be consid- A multidisciplinary approach causes more ered as the basis upon which other phenomena have conflicts. These conflicts, of course, are preferable to built (Snoeks, in press), resulting in the present day the false feeling of confidence based on a one-sided distributions, Lake Malawi/Nyasa apparently has never passed through su ch a stage of major vicariant JouRNAL OF AQUARICULTURE AND AQUATIC SCIENCES events. Still it is possible that at one stage two isolated CICHLID RESEARCH: STATE OF THE ART subbasins [one small in the north-eastern part of the VoLUME IX lake and one more southwards on the western shore] Page 161 approach, but they do have the terrible habit of Mark Hanssens (Tervuren) and Ron Coleman (Sacra­ enhancing the complexity of the taxonomie data set mento) for reviewing the text and for suggestions for available. And ofcourse, each approach urges a certain improvement. I benefitted from discussions with Tom claim of producing the most reliable results. In an Johnson (Minnesota) and Sven Kullander (Stockholm). ongoing study on the Ophthalmotilapia from Lake Tanganyika (Hanssens et al., 1999; in prep.), it was REFERENCES found that the various approaches, morphometry, the Cohen, A.S., M.J. Soreghan, and C.A. Scholz, analysis of the color patterns, and the sequencing of 1993. 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