Species Distinction and the Biodiversity Crisis in Lake Victoria

Transcription

1 Transactions of the American Fisheries Society 136: , 2007 Ó Copyright by the American Fisheries Society 2007 DOI: /T [Article] Species Distinction and the Biodiversity Crisis in Lake Victoria F. WITTE* Institute of Biology, University of Leiden, Post Office Box 9516, 2300 RA, Leiden, The Netherlands J. H. WANINK Institute of Biology, University of Leiden, Post Office Box 9516, 2300 RA, Leiden, The Netherlands; and Koeman en Bijkerk BV, Ecological Research and Consultancy, Post Office Box 14, 9750 AA Haren, The Netherlands M. KISHE-MACHUMU Institute of Biology, University of Leiden, Post Office Box 9516, 2300 RA, Leiden, The Netherlands; and Tanzania Fisheries Research Institute, Post Office Box 78850, Dar es Salaam, Tanzania Abstract. Until the 1970s, the fish fauna of Lake Victoria in East Africa was dominated by about 500 endemic haplochromine cichlid species, which comprised about 80% of the demersal fish mass. The cichlids were extremely diverse ecologically; however, the small diversity in gross morphology and the presence of intraspecific variation made it difficult to distinguish among species. In the first half of the 1980s, the Nile perch Lates niloticus, an introduced predator, suddenly boomed and cichlids declined dramatically. During the same period eutrophication increased strongly. With the decline of Nile perch catches in the 1990s, the cichlids showed some recovery. These events have triggered many studies and debates. Disagreements about the severity and causes of the decline often stemmed from considering the cichlid flock as a single unit owing to the lack of proper taxonomic and ecological knowledge. By studying cichlid communities, trophic groups, and individual species, researchers uncovered differential impacts that helped them to unravel the causes of the changes. It seems that lakewide Nile perch predation and eutrophication had the strongest impact and that the fishery only had a local effect. Knowledge of the differential decline and recovery of the haplochromine cichlids and the underlying causes is important for the proper management of biodiversity and the fishery in Lake Victoria. Consequently, knowledge of the systematics of cichlids is a key issue in managing the lake. Lake Victoria is the largest tropical lake in the world (Fryer and Iles 1972), having a surface area of about 68,800 km 2 and a maximum depth of about 70 m. The lake is situated at an altitude of 1,134 m above sea level and is bordered by Tanzania, Kenya, and Uganda (Figure 1). Lake Victoria originated less than 1 million years ago and may even have been dry for several millennia until about 14,000 years ago (Johnson et al. 1996; but see Fryer 2004). In spite of its young age, the lake originally had an extremely rich fish fauna, comprising several hundred species of cichlids (Greenwood 1974; Witte and van Oijen 1990; Seehausen 1996; Kaufman et al. 1997), 17 cyprinid species, 10 catfish species belonging to four families, and 19 other species divided among six families (Greenwood 1974; van Oijen 1995). During the last century, the commercial fishery in Lake Victoria resulted in overfishing of some of the target species, especially the tilapiine cichlids (Fryer and Iles 1972; Ogutu-Ohwayo 1990). Therefore, exotic fish species were introduced into the * Corresponding author: f.witte@biology.leidenuniv.nl Received July 7, 2005; accepted May 18, 2006 Published online July 5, 2007 lake in the 1950s to support the fishery. They included the Nile tilapia Oreochromis niloticus, a detritivore, and the Nile perch, Lates niloticus, a large predator. A lakewide bottom trawl survey in revealed that 80% of the demersal fish mass consisted of haplochromine cichlids (Kudhongania and Cordone 1974). To exploit the abundant small haplochromines, a bottom trawl fishery was started in 1976 in the vicinity of Mwanza (Figure 1). Catch rates were 1,000 1,500 kg/h, and about metric tons of haplochromine fishes per day were converted into fish meal for fodder. Within a couple of years, signs of local overfishing became apparent (Witte and Goudswaard 1985). At the beginning of the 1980s the Nile perch population suddenly expanded and dramatic changes in the catches were observed; haplochromines in the sublittoral and offshore areas vanished almost completely (Barel et al. 1985, 1991; Ogutu-Ohwayo 1990; Witte et al. 1992). At about the same time blooms of blue-green algae increased greatly due to eutrophication (Ochumba and Kibaara 1989; Hecky 1993; Mugidde 1993; Verschuren et al. 2002) This resulted in decreased levels of dissolved oxygen (Kaufman 1992; Hecky et al. 1994; Wanink et al. 2001) and decreased water transparency 1146

2 SPECIES DISTINCTION IN LAKE VICTORIA 1147 FIGURE 1. Map of Lake Victoria, indicating the study sites and the main sampling stations. (Seehausen et al. 1997a; Witte et al. 2005). Sediment cores indicated that eutrophication of the lake had already begun in the 1920s (Hecky 1993; Verschuren et al. 2002). In the 1990s, after a decline of Nile perch populations due to heavy fishing, a slow resurgence of some haplochromine species was observed (CIFA 1990; Witte et al. 1995, 2000; Seehausen et al. 1997b; Balirwa et al. 2003; Getabu et al. 2003). The Nile perch upsurge, the dramatic decline of the haplochromine cichlids, and other ecological changes in Lake Victoria triggered many studies and debates about the extent and the causes of these changes (e.g., Barel et al. 1985, 1991; Coulter et al. 1986; Ribbink 1987; Anonymous 1987; Seegers 1987; Acere 1988; Harrison et al. 1989; Ogutu-Ohwayo 1990; Kaufman 1992; Kudhongania et al. 1992; Witte et al. 1992, 1995; Hecky et al. 1994; Bundy and Pitcher 1995; Seehausen et al. 1997a, 1997b, 2003; Harrison and Stiassny 1999; Verschuren et al. 2002; Gurevitch and Padilla 2004). However, in many of these studies the haplochromine cichlids were considered as one unit because it is very difficult for nonspecialists to identify these fish to the species level or even higher levels, such as trophic groups or genera. We hypothesize that identification of this speciose group to the species level is helpful in unraveling what happened in Lake Victoria and crucial for the proper management of its fishery and biodiversity. Methods Sampling techniques. Haplochromine cichlids were studied in the littoral and sublittoral waters of the Mwanza Gulf. Eleven stations on a research transect across the Mwanza Gulf were monitored between 1979 and The research transect is

3 1148 WITTE ET AL. approximately 5 km wide and has a depth of 2 15 m (Figure 1). A small trawler, powered by a 20- or 25-hp outboard engine (1 hp ¼ 746 W), was used for bottom and surface trawling (bottom trawl: headrope, 4.6 m; cod-end mesh, 5 mm; surface trawl: beam, 4.5 m; codend mesh, 5 mm). Trawls at each station lasted 10 min. Larger trawlers ( hp; headropes, m; cod-end mesh, 20 mm) were used to sample the Mwanza Gulf, Speke Gulf, Emin Pasha Gulf, and deepwater stations (40 60 m). At station G (13 15 m deep; Figure 1), gill nets were set at the bottom, the middle and the top of the water column. The nets were 60 m long and 1.5 m deep and composed of six panels of 10 m each, with mesh sizes of 2.5, 3.8, and 5.1 cm. Rocky shores were fished with gill nets, local traps, and angling rods baited with worms. Catches were stored on ice and afterwards analyzed in the laboratory for species and trophic composition. Only adult or subadult fish (generally.4 cm standard length [SL]) were used to determine the trophic composition. Species distinction. Distinguishing species in the relatively young haplochromine species flock of Lake Victoria is a complex matter. Interspecific differences in morphology are often extremely small (Greenwood 1974; Barel et al. 1977). At the same time, a great deal of intraspecific variation, comprising ontogenetic changes, sexual dimorphism, phenotypic plasticity, and color polymorphism, has been found (Witte et al and references therein). Male coloration appears to play an important role in the specific mate recognition system (SMRS; Paterson 1980) of Lake Victoria cichlids. Haplochromine cichlid males are brightly colored, and females appear to actively select males according to coloration (Seehausen and van Alphen 1998). Witte et al. (1997) considered groups of haplochromines to belong to two different species if, in sympatry, they are distinguishable in terms of male coloration and other characters and have few or no intermediates, indicating that there is little or no gene flow between them. This is similar to the genotypic cluster definition of Mallet (1995). However, both phenotypic plasticity and geographic variation make it difficult to distinguish between species in allopatric or allochronic situations. In such cases, characters involved in the SMRS were considered decisive. Seehausen et al. (1998a) made the definition more precise. The likelihood that one is dealing with sibling species is considerably larger when two groups differ in more than one genetically independent trait. Therefore, they suggested in agreement with the genotypic cluster definition of species (Mallet 1995), to diagnose haplochromine species by correlated presence and absence of states in (at least two) genetically independent characters. Trophic groups. Lake Victoria cichlids are often classified into trophic groups (Greenwood 1974; van Oijen et al. 1981; Witte 1981; Witte and van Oijen 1990; Kaufman and Ochumba 1993; Seehausen et al. 1997b). A trophic group consists of species using the same food category. However, many species feed on several types of food. In these cases the dominant food category is taken as decisive for the trophic classification (e.g., Witte 1981). Species within a trophic group generally share morphological characters that are related to the uptake and processing of their dominant food source (Greenwood 1974; Witte and van Oijen 1990). In some cases subgroups can be identified on the basis of food processing, the location of the food, or the part of the prey that is eaten. For example, within the molluscivores, pharyngeal crushers use their pharyngeal jaws to crush the shell, whereas oral shellers or crushers feed on snails by wrenching the body from its shell or by crushing the shell with their oral jaws. Within piscivores one can distinguish between piscivores in the strictest sense (which feed on whole fish) and other members of this trophic group, such as scale eaters and pedophages (which feed on fish eggs and larvae). Greenwood (1979, 1980) revised the Lake Victoria haplochromine fish, splitting them into more than 20 genera and subgenera. In addition, Seehausen et al. (1998a) described three new genera of rock-dwelling cichlids. During the past decades there have been extensive debates on the validity of the genera defined by Greenwood (Hoogerhoud 1984; Meyer et al. 1990; Lippitsch 1993; Snoeks 1994; Seehausen 1996; van Oijen 1996; Seehausen et al. 1998a). Because of the disagreements, and as a considerable number of the haplochromine species from Lake Victoria cannot be assigned to the new genera, we prefer to keep the species in the genus Haplochromis and add the new generic names in parentheses, (i.e. use them as subgenera). For species that cannot be assigned to any of the new genera, the name Haplochromis is followed by (?). The morphological characters used by Greenwood (1979, 1980) for his revision of the genus Haplochromis show considerable overlap with those that characterize the trophic groups. Consequently, the trophic classification we use in this paper corresponds broadly with the genera proposed by Greenwood (1979, 1980) (see Table 1). Results and Discussion Species Discovery and Description Three periods can be recognized in the discovery and description of the Lake Victoria haplochromine cichlid species (Figure 2). The first comprises the time

4 SPECIES DISTINCTION IN LAKE VICTORIA 1149 TABLE 1. Haplochromine (sub)trophic groups, the genera proposed by Greenwood (1979, 1980) and Seehausen et al. (1998a) as comprising the trophic groups, the size ranges of the adult fish, the number of described species, and the total number of species collected in Lake Victoria. Number of species Trophic group Proposed genera a SL (cm) Described Total Detritivores Enterochromis Phytoplanktivores? Algae grazers Epilithic Neochromis, Mbipia Epiphytic Haplochromis, Xistychromis Plant eaters Xistychromis, Psammochromis Molluscivores Pharyngeal Labrochromis, Astatoreochromis Oral Ptyochromis, Hoplotilapia, Macropleurodus, Paralabidochromis, Platytaeniodus Zooplanktivores Open water Yssichomis, Astatotilapia Rocks Lithochromis, Pundamilia Insectivores Astatoreochromis, Paralabidochromis, Psammochromis, Gaurochromis, Pundamilia Prawn eaters Prognathochromis Crab eaters Harpagochromis Piscivores Whole fish b Harpagochromis, Prognathochromis, Pixychromis Pedophages Lipochromis Scale eaters Allochromis Parasite eaters? Sponge eaters Pundamilia Unknown 5 57 Total a The genera to which most of the species in a given trophic group are allocated are indicated by bold italics. b Piscivores in the strict sense. between 1888 and 1938, when cichlids were collected during expeditions and afterwards described by museum taxonomists. A total of 61 species were described during this period but little or no data were available on live colors and ecology. The second period ( ) saw the publications of P. H. Greenwood, who worked from 1951 to 1957 as a Fisheries Research Officer in the northern part of the lake. His studies were mainly done in littoral habitats that were fished with gill nets and beach seines. He described many new species and redescribed most species from the earlier publications (see papers reprinted in Greenwood 1981). By 1969, 104 species had been described (Figure 2). During his field work, Greenwood collected data on ecology and coloration from live fishes. The third period, which started in 1975, is characterized by the ecological field work of the Haplochromis Ecology Survey Team of Leiden University and other researchers in the southern part of the lake. Until 1990, their work concentrated on sublittoral and offshore waters in and near the Mwanza Gulf (Figure 1), where a commercial trawl fishery had commenced (van Oijen et al. 1981). After the disappearance of the haplochromines from these habitats (Barel et al. 1991; Witte et al. 1992), the ecological studies focused on rock-dwelling cichlids (e.g., Seehausen et al. 1997a, 1998b; Bouton et al. 1999). Based on the species already described, undescribed taxa from museum collections, and information from FIGURE 2. Number of described haplochromine cichlid species and total number of haplochromine species known from Lake Victoria. Species in group A were described by taxonomists who did not work in the lake, those in group B by Greenwood (northern part of the lake), and those in group C by the Haplochromis Ecology Survey Team and other workers (southern part of the lake). The total numbers of species are based on the following data: 1 ¼ Greenwood (1974), 2 ¼ van Oijen et al. (1981), 3 ¼ Witte et al. (1992), 4 ¼ Kaufman and Ochumba (1993), 5 ¼ Seehausen et al. (1997b), and 6 ¼ Seehausen (1999).

5 1150 WITTE ET AL. the workers that sampled new areas, Greenwood (1974) estimated that in all there were haplochromine species in Lake Victoria. This number increased substantially during the surveys in the southern part of the lake (Figure 2). In the Mwanza Gulf alone, more than 100 new species were discovered between 1977 and 1981, increasing the total number of species to about 250 (van Oijen et al. 1981). A trawl survey in 1985 in the southwestern corner of the lake, covering roughly the area between the Mwanza Gulf and Bukoba, yielded more than 50 new species (Witte et al. 1992). This survey was made at the start of the rapid Nile perch population expansion. Only a year later, catches were dominated by Nile perch in these areas (Goudswaard and Ligtvoet 1988). Data gathered between 1989 and 1993 by members of the Lake Victoria Research Team in Kenya and Uganda resulted in 31 new species (Kaufman and Ochumba 1993). It should be noted, however, that some of these came from satellite lakes. Surveys in the Mwanza and Speke gulfs during the first half of the 1990s added another 100 new species, mainly rock dwellers, to the list (Seehausen 1996; Seehausen et al. 1997b). By 1997, at least 436 species had either been described or given chironyms (Table 1). Since that time, the estimated number of species has grown to more than 500 (Seehausen 1999). Several authors raised doubts about the taxonomic status of Lake Victoria cichlids (Sage and Selander 1975; Turner and Grosse 1980; Crapon de Caprona and Fritzsch 1984; Meyer 1987). However, in many cases ecological research has corroborated the biological soundness of species distinctions based on male coloration and small morphological differences. That is, no indications of gene flow could be found between presumed species that lived in sympatry (Hoogerhoud et al. 1983; Goldschmidt and Witte 1990; Seehausen et al. 1998b). Trophic Groups At least 15 (sub)trophic groups have been identified among the Lake Victoria haplochromine fish. The number of species per trophic group differed considerably. Piscivores in the strictest sense comprised the highest number of species, and insectivores the next highest (Table 1). In terms of biomass, however, a completely different picture emerged; detritivores dominated the catches in the sublittoral waters, comprising 38% of total biomass, whereas piscivores made up only 6% (Goldschmidt et al. 1993). The trophic groups are not equally distributed throughout the lake. For instance, epilithic algae grazers are restricted to rocky shores and epiphytic algae grazers are caught mainly along shores with stands of rooted plants (e.g., Greenwood 1974; Witte et al. 1992; Seehausen et al. 1997b). Insectivores and oral-shelling molluscivores are mainly associated with hard substrates like sand and rocks and detritivores with mud bottoms (e.g., Greenwood 1974; Witte 1981; Witte et al. 1992). Even at a single station (e.g., station G), trophic groups and species are not equally distributed (Figure 3). Detritivores, insectivores, and molluscivores are mainly bottom dwellers, whereas phytoplanktivores are typically surface dwellers. Zooplanktivores, piscivores, and prawn eaters occupy the whole water column; some species live close to the bottom while others are more pelagic. Many species, especially zooplanktivore species, move higher into the column during the night (Figure 3). Haplochromine Communities Owing to the restriction of many species to certain bottom types, depths, or parts of the water column, the haplochromine cichlid flock of Lake Victoria can be subdivided into different communities; bottom substrate appears to be a major factor in demarcating such communities. Fish communities over rock, sand, and mud bottoms are strikingly different from one another (Greenwood 1974; van Oijen et al. 1981; Witte 1981; Seehausen 1996; Seehausen et al. 1997b). The small (,0.5 km 2 ) and shallow (,7 m) Butimba Bay (Figure 1) provides an example. Monthly samples with a bottom trawl at stations A D during the period February 1979 July 1980 revealed 81 haplochromine species in total. The sand habitat harbored more species (75 species) than the mud habitat (49 species). Thirtytwo species were caught only over sand, 6 only over mud, and 43 over both substrate types. Other habitats, the rock pebble sand bottoms and the rock reed interface, each with its own group of species, were also distinguished (Seehausen et al. 1997b). The difference in species composition in different habitats can be partly explained by the availability of habitat-related food sources. For instance, rocks in water where sufficient light penetrates are covered with epilithic algae. These algae (including their associated nonattached fauna) are cropped by specialized epilithic algae grazers (Fryer and Iles 1972; Seehausen 1996; Seehausen et al. 1998a). Likewise, areas with submerged vegetation harbor epiphytic algae grazers (Fryer and Iles 1972; Greenwood 1974; Witte and van Oijen 1990). The presence or absence of food type, however, is not the only factor that may play a role in determining species distribution. For instance, abiotic environmental conditions may have an impact on feeding performance. In laboratory experiments, the feeding efficiency of oral-shelling molluscivores decreased strongly with declining light conditions, whereas this was not the

6 SPECIES DISTINCTION IN LAKE VICTORIA 1151 FIGURE 3. Mean catch rate of haplochromine cichlids by trophic group (detritivores, phytoplanktivores, zooplanktivores, insectivores, molluscivores, piscivores, and prawn eaters) in gill nets set at the surface, in midwater, and at the bottom at station G (15 m deep). Catches were made during 8 d (top panel) and 8 nights (bottom panel) in the period August 1981 June Whiskers represent SDs. Note that among the zooplanktivores and the piscivores there are species that are more benthic and species that are more pelagic. case for the feeding efficiency of pharyngeal mollusk crushers (M. Rensing and F. Witte, unpublished data). This difference may explain why oral shellers were mainly caught over hard substrates (rock and sand) with relatively clear water, whereas there was no significant difference in the distribution of pharyngeal mollusk crushers over sand and mud, either in number of individuals or number of species (Greenwood 1974; F. Witte, unpublished data). Depth also seems to be an important variable in determining species distribution. Actually, depth itself may not be the main explanatory factor but rather depth-related factors like light conditions and dissolved oxygen concentrations (e.g., Hoogerhoud et al. 1983). Based on his research in the northern part of the lake, Greenwood (1974) recognized three depth-related habitats: littoral regions (,6 m), sublittoral regions (6 20 m), and deepwater regions (.20 m). But, he added that they are rather more artificial than natural categories and that they tend to intergrade with one another. Nevertheless, catch compositions over mud bottoms in the Mwanza Gulf confirm Greenwood s (1974) classifications; though the species composition gradually changes with depth, there are species that typically occur in bays (,6 m) and others that are characteristic of the main body of the gulf (6 20 m). Finally, a distinction can be made between bottomdwelling and pelagic cichlid communities, the latter being dominated by phytoplanktivorous, zooplanktivorous, and piscivorous species (Figure 3; van Oijen et al. 1981; van Oijen 1982; Goldschmidt et al. 1990, 1993; Witte et al. 1992). Is the Biodiversity Crisis in Lake Victoria Real? As mentioned in the introduction, there has been a dramatic decline in Lake Victoria haplochromines during recent decades (Figures 4, 5; Barel et al. 1985; Ogutu-Ohwayo 1990; Witte et al. 1992). Of 123

7 1152 WITTE ET AL. FIGURE 4. Declines in the percentage of haplochromine species caught over rocks, in littoral habitat (,6 m), and in sublittoral habitat (6 20 m) in the northern part of the Mwanza Gulf from the end of the 1970s to end of the 1980s. The total number of species caught in each habitat before the decline is given above the bar (based on data in Witte et al. 1992). FIGURE 5. Mean number of haplochromine cichlids in catches of 10 min duration with a small bottom trawler at species collected during the period at the research transect, about 80 had disappeared by From this observation it is estimated that in the sublittoral and offshore waters of the lake about 200 haplochromine species have disappeared or been threatened with extinction (Witte et al. 1992). Harrison and Stiassny (1999) criticized this estimate by noting that it is probably injudicious to assume a species of Lake Victoria cichlid is extinct simply because it has not been collected for a few years in a particular region. Further, they noted that an additional problem is the assumption that just because a species has disappeared from the Mwanza Gulf it is not present elsewhere in another part of the lake. They suggest following the more rigorous approach of Diamond (1987), who presumed a species to be extant unless proven extinct and to use the term extirpated to denote regional extinction. Other authors have disputed the seriousness of the decline or disagreed about the causes (Anonymous 1987; Seegers 1987; Acere 1988; Harrison et al. 1989; Kudhongania et al. 1992; Hecky et al. 1994; Bundy and Pitcher 1995; Verschuren et al. 2002). As we will demonstrate below, these disagreements often stemmed from considering the haplochromine flock as a single unit owing to the lack of taxonomic and ecological knowledge. In the 1990s, catches of haplochromines showed some recovery (e.g., Witte et al. 1995, 2000; Seehausen et al. 1997b), but again, no differentiation was made among species in some papers (e.g., CIFA 1990; Getabu et al. 2003). In the following sections, knowledge of species communities, trophic groups, and individual species will be used to analyze the decline and recovery of haplochromines. stations G J in the Mwanza Gulf during Whiskers represent SDs. For 1979, 1981, and 2005, SDs are given as numbers above the bars. Detritivores and zooplanktivores are the two most abundant trophic groups in this area. Differential Impacts on Communities Shortly after the first reports on haplochromine decline in Lake Victoria (Barel et al. 1985; Coulter et al. 1986), some papers appeared claiming that the decline had been exaggerated (Anonymous 1987; Seegers 1987; Harrison et al. 1989). These authors based their view on samples taken from the littoral communities that are easily accessible with beach seines and gill nets. However, when considering the different haplochromine communities in the Mwanza Gulf, the relative decline of haplochromine species appears to have increased with depth. In 1987, more than 90% of the species of the sublittoral community had disappeared (Figure 4). For the littoral communities over sand and mud bottoms, the decline in species was about 70%, whereas for the rock-dwelling community it was less than 40%. So, the abovementioned authors studied communities that were less affected than those further offshore. Moreover, these researchers had no information on the previous species composition in those areas. The pattern of species decline in different cichlid communities (Figure 4) was opposite to that of the distribution of Nile perch (.25 cm total length) in the Mwanza Gulf. Catch rates of these piscivorous Nile perch rose by a factor of 10 from the shallow (1 2 m) littoral areas in the south of the Mwanza Gulf to the deeper (20 25 m) areas at its entrance (Goudswaard et al. 2002). Until 1986, when it was stopped, the trawl

8 SPECIES DISTINCTION IN LAKE VICTORIA 1153 fishery was common in sublittoral areas of the Mwanza Gulf. Consequently, it may have contributed to the decline of the haplochromine community in these areas. However, in areas without an intensive haplochromine fishery but with high Nile perch densities, such as the deep-water sampling stations and the Emin Pasha Gulf, declines of haplochromine fish similar to those of the Mwanza Gulf were found (Witte et al. 1992, 1995; Goudswaard 2006). Moreover, these studies revealed a remarkable coincidence of Nile perch increase and haplochromine decline in various areas of the lake. This seems to corroborate the impact of Nile perch. However, the effect of less water transparency and lower dissolved oxygen levels from eutrophication cannot be ruled out, as limnological data for these areas are not available. Least affected were the haplochromine communities from rocky shores (Figure 4). It is likely that haplochromine fish living between boulders and in crevices are relatively protected from Nile perch predation. More than half of the species that did disappear from rocky habitats were not restricted to rocks or only lived at their periphery (Witte et al. 1992). The strong exploitation of rock-dwelling fish for longline bait and the application of insecticides for fishing at rocky islands may provide explanations for the local species declines that were observed at a later stage (Seehausen et al. 1997b). Eutrophication probably also played a role in the decline of haplochromine species in rocky habitats. A number of species that disappeared from the Mwanza Gulf were later rediscovered adjacent to islands in the Speke Gulf, where water transparency was higher (Seehausen et al. 1997a, 1997b). Differential Impacts on Trophic Groups To study the impacts at the trophic group and species levels, we will focus on the sublittoral community at stations G J in the Mwanza Gulf because these stations were most affected and because they were sampled most frequently during the past decades. If haplochromines were considered as a single unit, our data would only demonstrate a strong decrease in the catch between 1979 and 1988 and a subsequent rise in the next 17 years (i.e., the total number of individuals in Figure 5). However, a more detailed study of the decline of the sublittoral haplochromines reveals differential impacts at the trophic group level. For instance, trophic groups comprising mainly largesized species like piscivores, molluscivores, and insectivores (Table 1), declined faster than those comprising small species (Witte et al. 1992, in press). The size selectivity of trawl nets and Nile perch could be the cause of this differential decline. Besides these size-related differences, there were differences in the decline and resurgence of trophic groups that comprise only small species, namely, the zooplanktivores and the detritivores. The decline of the zooplanktivores was less steep and their resurgence was faster than that of the detritivores (Figure 5). Currently, the densities of zooplanktivores are higher than they were before the ecological changes, whereas those of detritivores are much lower than at that time. A tentative explanation for the difference is that bottom trawling and the bottom-dwelling Nile perch had less impact on the partly pelagic zooplanktivores than on the bottomdwelling detritivores. The slow recovery of the detritivores, however, cannot be attributed to the effect of the trawl fishery, as this fishery was stopped in Nile perch catches declined after 1987, but they still dominate the fish mass in the Mwanza Gulf (Witte et al. 2000, in press), and the first algal blooms in this area were observed in 1986 (J. H. Wanink, personal observation). Thus, Nile perch predation and the impacts of eutrophication are the most likely explanations for the differences in recovery between zooplanktivores and detritivores (Witte et al., in press). Differential Impacts on Species Within trophic groups, there appeared to be differences in the rate of decline. Large piscivorous species disappeared faster than small ones (Witte et al. 1992, 2005) and most of these larger species did not recover (Table 2). The only piscivore that we caught on the research transect in the period was a species of less than 10 cm SL. This observation further supports the suggestion that the differential decline was at least partly size related. But there are also interspecific differences that are independent of size. When one looks at the zooplanktivores more closely, it appears that although the number of individuals recovered to its original level (Figure 5), the species composition was different. In the period , at least 12 species were caught at the stations G J (Table 2), of which the four most common ones were Haplochromis (also known as Yssichromis) pyrrhocephalus, H. (Y.) heusinkveldi, H. (?) piceatus and H. (?) argens. In 2005 eight species were caught, of which H. pyrrhocephalus, H. (Y.) laparogramma, and H. (?) tanaos were common. Haplochromis heusinkveldi and H. piceatus were abundant at the research transect in the past but have not been caught there or elsewhere since their disappearance in Before the ecological changes, H. laparogramma primarily occurred in deep water outside the Mwanza Gulf (Goldschmidt et al. 1990), while H. tanaos seemed restricted to shallow sand bottoms (van Oijen and Witte 1996; Seehausen et al. 1997b). Both species are now common in the

9 1154 WITTE ET AL. TABLE 2. Numbers of species collected at stations G J in the northern part of the Mwanza Gulf in three periods: (1) before the ecological changes ( ); (2) when haplochromine catches were lowest ( ); and (3) after the recovery of some species ( ). The numbers in parentheses indicate that species were not present at stations G J but were still occasionally found at other sites (data of and from Witte et al. 1992). Trophic group Detritivores 11 0 (4) 5 Phytoplanktivores 2 0 (1) 0 (1) Epiphytic algae grazers 2 0 (2) 0 (1) Molluscivores Pharyngeal 5 0 (1) 1 Oral 2 0 (1) 2 Zooplanktivores 12 3 (2) 8 Insectivores 5 0 (1) 0 (1) Prawn eaters Piscivores Whole fish Pedophages Scale eaters Parasite eaters Unknown Total 67 4 (12) 18 (3) sublittoral part of the research transect, though H. tanaos mainly occurs at the shallower stations (I and J). Haplochromis pyrrhocephalus is now more abundant than in the 1970s and has even extended its habitat to areas that were dominated by H. piceatus in the past. A comparison of closely related species that have responded differently to the environmental changes may be helpful in unraveling causes of differential extirpation and survival. The species pair H. heusinkveldi and H. pyrrhocephalus provides an example. These two species had almost identical distribution and migration patterns and were equally abundant before the Nile perch boom. Yet H. heusinkveldi vanished and H. pyrrhocephalus became the most common species in the Mwanza Gulf. Morphologically, the two species differed in retinal structure (van der Meer et al. 1995), and the eyes of H. pyrrhocephalus are better adapted to low-light conditions whereas those of H. heusinkveldi are better for seeking out small prey items. Ecologically, the species differed in diet (Goldschmidt et al. 1990) and in spawning period (Goldschmidt and Witte 1990). In contrast to H. pyrrhocephalus, H. heusinkveldi included phytoplankton in its diet and had a spawning period limited to months with high water transparency. The eyes of H. heusinkveldi have the ability to see details at a high resolution, which would make them suited to feed on phytoplankton but may have hampered spawning under low-light conditions. Thus, in addition to Nile perch predation, the reduced water clarity in the 1990s may have hampered the recovery of H. heusinkveldi (Witte et al. 2000). In contrast, the adaptations to low light intensities may have played a role in the successful recovery of H. pyrrhocephalus when Nile perch densities decreased. Adaptive Responses in Recovering Species The study of H. pyrrhocephalus and H. heusinkveldi suggests that light conditions played a role in the decline and resurgence of haplochromine fish. A morphological study of the eyes of H. tanaos, which used to be restricted to shallow sand bottoms (e.g., stations A and B) but is now common over mud bottoms up to 10 m, revealed adaptations to the decreased light conditions in the lake and to the habitat shift. The retina of this species adapted to the lower water clarity and the related shift of the ambient light toward longer wave lengths (Seehausen et al. 2003; Witte et al. 2005). The size and density of the bluesensitive single cones decreased, whereas that of the red green-sensitive double cones increased (L. Wagenaar, H. J. van der Meer, J. H. Wanink, and F. Witte, unpublished data). This observation raises the question why, if our hypothesis about the cause of the disappearance of H. heusinkveldi is correct, it failed to adapt to the new environment. So far we have no satisfactory explanation. Morphological changes in the gills were also found in H. pyrrhocephalus sampled during the 1990s. The average gill surface was about 70% larger than that of fish sampled during the 1970s (M. Welten, J. H. Wanink, and F. Witte, unpublished data). Even more striking, we found species that we had never seen before during the 25 years of our lake studies. There are several hypotheses for the fast emergence of morphological changes and new species : (1) invasions of populations from other areas were not as well studied in the past; (2) the anatomy or coloration of the fishes that inhabit the area changed in direct response to the environmental changes (phenotypic plasticity); (3) the new morphological variations represent hybrids or hybrid descendants; (4) genetic changes have taken place in the small surviving populations; and (5) some combination of these factors was at work. Currently, we are doing experiments on phenotypic plasticity and genetic studies on conspecific populations from the 1970s and 1990s to test these hypotheses. Conclusions Our study demonstrates that knowledge of the systematics of haplochromine cichlids is crucial for the management of both the biodiversity and the fish production of Lake Victoria. The biodiversity crisis in the lake might have remained largely unknown if species inventories had not been carried out in the

10 SPECIES DISTINCTION IN LAKE VICTORIA s and 1980s in the sublittoral and offshore waters just before and during the dramatic decline of the cichlid species (Figures 2, 5). Many of the species discovered in those years in the sublittoral and offshore waters of the Mwanza Gulf had disappeared by the end of the 1980s. Since the 1990s, the abundance of haplochromines has again increased; however, the number of species is lower and the trophic composition has changed (Figure 5; Table 2). A few species were rediscovered in habitats where they were formerly absent or less common (Witte et al. 1995; van Oijen and Witte 1996; Seehausen et al. 1997b; J. H. Wanink and F. Witte, personal observations). This gives hope that more species survived in refugia (Kaufman and Ochumba 1993; Seehausen et al. 1997b). Similar observations were made in Lake Nabugabo (Chapman et al. 1996). Nevertheless, the sampling of many habitats during the past 18 years yielded only a few of the more than 200 species that we estimated to be lost. We agree with Harrison and Stiassny (1999) that to draw up an extinction list that can be viewed with some confidence it is necessary to set rigorous criteria. They suggested that one follow the approach of Diamond (1987), which presumed a species extant unless proven extinct. However, in a vast water body like Lake Victoria, in which the taxonomically complex cichlid communities have been studied only very locally to the species level, it may take decades before a proper inventory is made. Thus far, the research transect in the Mwanza Gulf is the only place where species composition has been studied over a long period. Still, local extirpation may be indicative of extinction, as an almost complete disappearance of the haplochromines in sublittoral and offshore waters was observed lakewide in the 1980s (Okemwa 1981; Goudswaard and Ligtvoet 1988; Ogutu-Ohwayo 1990; Barel et al. 1991; Okaronon 1994). Though we are aware that we may err in considering some species extinct, we are inclined to use the approach that according to Diamond (1987) is appropriate for more poorly known groups, that is, to treat them as extinct unless proven extant. This approach will probably not overestimate the number of extinctions in the lake. Rather, given the fact that in poorly studied areas new species were still discovered when haplochromine densities had strongly declined after the Nile perch expansion, it is likely that many unknown extinctions have occurred in Lake Victoria. The differential sensitivity to decline of haplochromine communities, trophic groups (or lineages), and species stresses that it is not valid to consider the haplochromine cichlids as a homogeneous unit. This holds not only for biodiversity assessments but also for fisheries management. For instance, the current selective recovery of zooplanktivores may have impacts on the ecosystem and the fishery in the lake. After the haplochromine decline in the 1980s, the biomass of the zooplanktivorous cyprinid, Rastrineobola (also known as Engraulicypris) argentea, increased substantially (Wanink 1991, 1999; Wanink and Witte 2000). Rastrineobola argentea extended its habitat and diet, including niche components that were formerly occupied by haplochromine species (Wanink and Witte 2000). This may have been caused by competitive release due to the decrease of the (zooplanktivorous) haplochromines. Consequently, the recent resurgence of zooplanktivorous haplochromines may, in turn, cause a decline of the R. argentea population, on which one of the major fisheries is currently thriving. Alternatively, an increase of the total zooplanktivorous ichthyomass (R. argentea and zooplanktivorous haplochromines) might decrease the zooplankton biomass and, through cascading effects, further enhance phytoplankton growth (Ogutu-Ohwayo and Hecky 1991). It should be noted, however, that the diet of H. pyrrhocephalus and H. tanaos has changed. After the ecological changes in the second half of the 1980s, they included larger prey in their diet and zooplankton became less important (van Oijen and Witte 1996; Katunzi et al. 2003). The same observations were made for the diet of R. argentea (Wanink and Witte 2000). For a true understanding of the changing ecosystem, the species composition of the resurging haplochromine communities should be monitored and the species positions in the food web studied. As demonstrated in this paper, the differential decline and resurgence that were found for haplochromine communities, trophic groups, and species help to unravel the causes of the changes. Fishing had an impact locally (especially on the larger species), but lakewide the decline must have been mainly due to Nile perch and eutrophication because large declines were also observed in lightly fished areas (Witte et al. 1995; 2005). Further, communities and trophic groups with a small habitat overlap with Nile perch declined more slowly than those with a large overlap. The impact of Nile perch is also evident from the resurgence of haplochromines after the decline of the Nile perch stock (Witte et al. 2000, 2005; Balirwa et al. 2003). The effect of eutrophication is indicated by the fact that, of two closely related species, the one that was best adapted to low-light conditions recovered, as well as by the adaptive responses to eutrophication in resurging species. This knowledge is important for management purposes. Nile perch seem to prefer and grow fastest on haplochromine prey (Kaufman and Schwartz 2002; Ogutu-Ohwayo 2004). Thus, it has

11 1156 WITTE ET AL. been suggested that sustainability in the Nile perch fishery could be maintained by a sufficient fishing pressure to ensure an abundance of haplochromine prey, but not so much pressure as to threaten the Nile perch stock itself (Balirwa et al. 2003). However, eutrophication, and especially the related low water clarity, may constrain cichlid diversity and abundance (Seehausen 1997a, 2003; Witte et al. 2005). Consequently, a decrease of eutrophication may increase haplochromine resurgence and help maximize Nile perch production rates. Management of Lake Victoria should therefore include provisions for halting and reversing eutrophication and for setting up reserves that typify various habitats of the lake (Balirwa et al. 2003). Banning the fishery and prohibition of further habitat degradation in such reserves may provide refugia for haplochromine species to some extent. Such reserves could function as sources from which other parts of the lake are seeded with haplochromines once the ecological conditions have improved in those areas. Clearly, the choice of reserves requires accurate knowledge of the composition of haplochromine species in the different areas. Unfortunately, many species have not yet been described formally and the number of trained taxonomists who could perform this task is low. In our opinion, taxonomic knowledge of Lake Victoria cichlids remains a key issue in managing the lake. Acknowledgments We thank our colleagues from the Haplochromis Ecology Survey Team (HEST), the Tanzania Fisheries Research Institute, and the Freshwater Fisheries Training Institute at Nyegezi for support and cooperation during the fieldwork. We thank the crews of the trawlers for their skilful labor. 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