The destruction of an endemic species flock : quantitative data on the decline of the haplochromine cichlids of Lake Victoria

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1 Environmental Biology of Fishes 4 : 1-28, Kluwer Academic Publishers. Printed in the Netherlands. The destruction of an endemic species flock : quantitative data on the decline of the haplochromine cichlids of Lake Victoria Frans Witte,' Tijs Goldschmidt,' Jan Wanink, 1 Martien van Oijen, 2 Kees Goudswaard, 1 Els Witte-Maas' & Niels Bouton' 1 Research Group on Ecological Morphology, Zoologisch Laboratorium, Rijksuniversiteit Leiden, I Postbus 9516, 2 00 RA Leiden, The Netherlands Nationaal Natuurhistorisch Museum, Postbus 9517, 2 00 RA Leiden, The Netherlands Received Accepted Key words : Extinction, Food web, Cichlidae, Nile perch, Overfishing, Predation, Species composition, Species introduction, Trophic groups Synopsis The Lake Victoria fish fauna included an endemic cichlid flock of more than 00 species. To boost fisheries, Nile perch (Lates sp.) was introduced into the lake in the 1950s. In the early 1980s an explosive increase of this predator was observed. Simultaneously, catches of haplochromines decreased. This paper describes the species composition of haplochromines in a research area in the Mwanza Gulf of Lake Victoria prior to the Nile perch upsurge. The decline of the haplochromines as a group and the decline of the number of species in various habitats in the Mwanza Gulf was monitored between 1979 and Of the 12 + species originally caught at a series of sampling stations ca. 80 had disappeared from the catches after In deepwater regions and in sub-littoral regions haplochromine catches decreased to virtually zero after the Nile perch boom. Haplochromines were still caught in the littoral regions where Nile perch densities were lower. However, a considerable decrease of species occurred in these regions too. It is expected that a remnant of the original haplochromine fauna will survive in the littoral region of the lake. Extrapolation of the data of the Mwanza Gulf to the entire lake would imply that approximately 200 of the 00+ endemic haplochromine species have already disappeared, or are threatened with extinction. Although fishing had an impact on the haplochromine stocks, the main cause of their decline was predation by Nile perch. The speed of decline differed between species and appeared to depend on their abundance and size, and on the degree of habitat overlap with Nile perch. Since the Nile perch upsurge, the food web of Lake Victoria has changed considerably and the total yield of the fishery has increased three to four times. Dramatic declines of native species have also been observed in other lakes as a result of the introduction of alien predators. However, such data concern less speciose communities and, in most cases, the actual process of extinction has not been monitored. Introduction 1989). It is therefore surprising that the study of extinction is one of the most neglected areas of ecology (Wilson 1988). During the past few dec- ades it has become increasingly clear that insight More than 99% of all species that have ever lived on Earth are now extinct (Prins & Hengeveld * Invited editorial

2 2 into the mechanisms which cause the rapid decline of populations or whole species is urgently needed to prevent extinction of threatened taxa (Kaufman 1986, Vermeij 1986). The large species flocks of cichlids in the Great African Lakes are unrivalled examples of vertebrate radiations (Fryer & Iles 1972, Greenwood 1974). Remarkably, the radiation of the monophyletic (Meyer et al. 1990) haplochromine species flock of Lake Victoria was achieved in the geologically short time span of years (Greenwood 1984). Since there are indications that the lake may have dried up more recently (Stager et al. 1986), this speciose flock even may be considerably younger. The trophic specializations of the endemic haplochromine cichlids have enabled them to exploit virtually all the food sources in the lake. The number of haplochromine species in Lake Victoria is estimated to have been more than 00 (Table 1). More than 80% of the demersal fish biomass consisted of these relatively small fishes (Kudhongania & Cordone 1974). In the 1950s and early 1960s Nile perch (Lates sp.) from Lake Albert and Lake Turkana were introduced into Lake Victoria (Hamblyn 1961, Arunga 1981, Welcomme 1988). Opposition to introduction of this predator had been expressed at the time (Fryer 1960a). During the following twenty years Nile perch were only caught in small quantities. In the early 1980s an explosive increase of Nile perch and a simultaneous decline of the stocks of most other fish species were reported for several areas of the lake (Arunga 1981, Okemwa 1981, Hughes 198, 1986, Barel et al. 1985, Goudswaard & Witte 1985, Okaronon et al. 1985, Goudswaard 1988, Goudswaard & Ligtvoet 1988, Ogutu-Ohwayo 1990a, 1990b, 1990c, Barel et al. 1991). Most striking was the dramatic decline of the previously abundant haplochromines (Hughes 198, 1986, Okemwa 1984, Barel et al. 1991). Apparently many of these endemic species were threathened with Preliminary taxonomic investigations of Lates specimens from Lake Victoria failed to identify these fishes unambiguously as L. niloticus (Harrison 1991, Witte personal observations). There remains the possibility that the Lates introduced into Lake Victoria belonged to other species, e.g. L. macrophthalmus or L. longispinis, or that Lates from Lake Victoria is a hybrid. extinction (Barel et al. 1985, Balon & Bruton 1986, Ribbink 1987). Since that time many articles appeared in newspapers, scientific and popular journals commenting upon the causes and seriousness of the decline of the haplochromines (e.g. Barel et al. 1985, various press cuttings in Barel 1986, Coulter et al. 1986, Seegers 1987, Anonymous 1987, 1988, Acere 1988, Harrison et al. 1989). However, none of these articles provided detailed quantitative data on the decline in species number, although in a few papers (Hughes 198, 1986, Okemwa 1984, Okaronon et al. 1985, Goudswaard & Ligtvoet 1988, Barel et al. 1991) data were presented on the decline of the haplochromines as a group. Fortunately, the haplochromines in the northern part of the Mwanza Gulf have been monitored at the species level over a time span of sufficient length to allow quantification of this process. In this paper we describe the species composition along a transect across the Mwanza Gulf, which was monitored from 1979 till We present data on : (1) the decline of the haplochromines as a group, (2) the decline of species in different habitats and ( ) the relative speed of disappearance of various species. We discuss interspecific differenc- Table 1. The trophic groups in Lake Victoria and their estimated species diversities. For sources and names of described species see Witte & van Oijen (1990). Trophic groups detritivores/phytoplanktivores phytoplanktivores epilithic algae grazers epiphytic algae grazers plant eaters pharyngeal mollusc crushers oral mollusc shellers/crushers zooplanktivores insectivores prawn eaters crab eater piscivores sensu stricto paedophages scale eater parasite eaters unknown Total Collected Described

3 es in rate of disappearance and the possible causes of the decline of the haplochromines. Our data strongly indicate that the majority of the haplochromine species in Lake Victoria have already disappeared or are threatened with extinction. We thus document the disappearance of a unique group of vertebrates. To provide a broader perspective, we compare our data with similar observations from other lacustrine environments into which predators have been introduced. Material and techniques Species recognition Species recognition was based on differences in male coloration and/or differences in morphology (Greenwood 1974, 1981, Barel et al. 1977, van Oijen et al. 1981, Witte & Witte-Maas 1987). For the identification of females morphological characters were more important, because the speciesspecific coloration of females was less distinct than that of males. Several examples of phenotypic plasticity in cichlids (Greenwood 1965, Witte 1984a, Hoogerhoud 1986, Witte et al. 1990) made clear that morphological differences, particularly between allopatric forms of the same trophic group, should be interpreted with caution (Witte & Witte- Maas 1987, cf. Meyer 1987). Thus, allopatric forms with similar male colorations were classified as conspecific, even though they differed to some extent in anatomical features (Witte & Witte-Maas 1987). On the other hand, anatomically similar forms which differed in male coloration were allocated to different species. We cannot rule out the possibility that some of these forms were colour morphs of a single species. However, ecological studies of a number of anatomically highly similar sympatric forms which differed distinctly in male coloration supported our approach to distinguishing species. Such sympatric forms showed differences in variables which are indicative of reproductive isolation, e.g. the location of spawning sites and the timing of breeding seasons (Hoogerhoud et al. 198, Witte 1984b, Goldschmidt et al. 1990, Goldschmidt & Witte 1990, Goldschmidt 1991). Individuals collected by the Haplochromis Ecology Survey Team (HEST) were compared with specimens of described species present in the Natural History Museum in London and in other museums. Undescribed species have been given cheironyms labelled by quotation marks in this paper. A reference collection of all species collected by HEST has been deposited in the Nationaal Natuurhistorisch Museum at Leiden, The Netherlands. Trophic groups Species were classified into trophic groups (Table 1 ; Greenwood 1974, van Oijen et al. 1981, Witte 1981, Witte & van Oijen 1990). Sometimes trophic groups were divided into sub-groups. Different criteria were used to make such subdivisions : (1) the place where the fishes obtained their food (e.g. epilithic algae grazers and epiphytic algae grazers) ; (2) the way in which the fishes processed their food (e.g. pharyngeal crushing molluscivores and oral shelling molluscivores) ; ( ) the part of the prey that was eaten (e.g. piscivores sensu lato, in this paper further referred to as piscivores, were divided into piscivores sensu stricto, paedophages and scale eaters). Species of which the diet was not known, were classified as `unknown'. Juveniles were also included in the calculations of the trophic composition, even though they may not yet have fed on the typical food source of the adults (cf. Witte 1981). Sometimes individuals could not be identified to the species level. These were recorded as 'unknown species' within the trophic group to which they belonged. Although the category `unknown species' most probably contains several species in each trophic group, they were considered as one species for each trophic group in our figures on species diversity. Sampling stations and sampling techniques Between 1977 and 1990 haplochromines were collected by HEST researchers in the Tanzanian waters of Lake Victoria (Fig. 1). To document the

4 4 Fig. 1. Study sites in Lake Victoria. The main sampling area of HEST for research on haplochromines was located in the Mwanza Gulf (see Fig. 2). Additional sampling was done in the Speke Gulf, the Emin Pasha Gulf, the Kagera Area and at a deepwater station north of Kome Island (see text). Winam Gulf is also called Kavirondo or Nyanza Gulf. changes in the haplochromine communities we used data from those areas in which we were familiar with the species composition. These areas comprised, among others, the research transect of HEST across the Mwanza Gulf and the rocky shores of a number of islands in the northern part of the Mwanza Gulf (Fig. 2 ; for details see van Oijen et al. 1981, Witte 1981). Monthly sampling of the transect started in February Stations H to K were not sampled after January 1980 and stations A, B, C, D and F were not sampled after July Stations E and G were sampled regularly until 1988 with an interruption in 1985/1986 (only four samples were taken at station G on ). In 1987, several catches were made over the whole transect. However, in this period the shallow stations A and B over sand were sampled in one tow ; the same holds for the shallow stations C and D with a mud bottom. In the present analyses these stations are combined as station A/B and station C/D respectively. In November 1990 stations A/B, C/D, E, F and G were sampled for the last time. Catches were made during the day with a small bottom trawler (20 hp, trawl net headrope 4.6 m, codend mesh 5 or 15 mm, see Witte 1981). Since several species were found to migrate to the surface at night (Witte 1984b, Goldschmidt et al. 1990),

5 5 additional sampling was done at night with a surface trawl (beam 4.5 m, codend mesh 5 mm) from 1981 onwards. Tows generally lasted 5-10 min. For each catch, a sample of kg, containing haplochromine cichlids, was identified to the species level. In order to compare catches, the number of fishes in the samples was scaled to trawl time. In 1987/1988 the total catch, which then consisted mainly of the cyprinid Rastrineobola argentea and young Nile perch, was screened for haplochromines. Data on the trawl catch rates of haplochromines in the Mwanza Gulf from 197 till 1986 were obtained from the Freshwater Fisheries Training Institute at Nyegezi. These catches were made with the research vessel Mdiria (120 hp, bottom trawl headrope 25 m, codend mesh 20 or 90 mm). Deepwater stations (40-60 m ; Fig. 1) were sampled from 1984 till 1989 with the research vessel Kiboko (105 hp, bottom trawl headrope 18 m, codend mesh 20 mm). Comparisons of catches of the small trawler and the Mdiria revealed that, at the beginning of the research period, the larger species (e.g. the piscivores sensu stricto of Witte & van Oijen 1990) were caught less frequently with the small gear. Catches along rocky shores of islands and the main coast were made between 1977 and 1982 and in 1990 using angling rods baited with earth worms, local fish traps and gill nets (25, 8 and 51 mm meshes). To compare the species composition at different depths before and after the decline, several stations and catch techniques were combined (Fig. 8). Stations A/B, C/D and BB were used for water depths of two to six metres, station E for depths of seven to eight metres, and station G and surroundings for depths of 1 to 15 metres. To determine the species composition before the decline, data were used from bottom trawl catches made by day in the period 1979/1980. Since no surface trawl data were available over the same period, we included data from nightly surface trawl catches (stations E, G) in 1981/1982. No surface trawl catches could be made at stations A/B and C/D due to the shallowness of the water. To determine the species composition after the decline, bottom trawl catches (stations A/B, C/D, E and G, in 1987/1988 and 1990), surface trawl catches (stations E, G in 1987/1988), and gill net catches (stations E, G, BB in 1987/1988) were used. In this case, data were used from all available catches irrespective of whether they were made during day or night. A gill net catch comprised nets ( 0 m long, 25 mm mesh) that were set at two or three different depths (bottom, midwater and surface) in the water column for approximately 12 h. The nets were hauled and emptied every four hours. Following Greenwood (1974), three depth regions are recognized : littoral (< 6 m), sub-littoral (6-20 m), and deepwater (> 20 m) (Fig. 1, 2). Results Number of haplochromine species prior to the decline Since 1981, when the number of haplochromine cichlids in Lake Victoria was estimated at more than 250 (van Oijen et al. 1981), more species have been discovered, most of them during a trawl survey in 1985 in the south west corner of the lake (Fig. 1 : Kome Island, Emin Pasha Gulf, Kagera area). Our current total amounts to 02+ (Table 1), only 119 of which have been described (Table 1 ; Greenwood 1981, Witte & van Oijen 1990). Using a variety of fishing techniques, more than 200 species were collected by HEST in the northern part of the Mwanza Gulf. Along the research transect (Fig. 2) 110+ species were encountered between 1979 and 1982 in the samples of bottom and surface catches with the small trawler (Table 2, Appendix 1, 2). Together with the haplochromines caught by angling and trapping at the rocks (Table, Appendix ), the total number of species that were recorded along the transect and the nearby rocky shores amounts to at least 12. Species diversity along the transect prior to the decline The distribution of the species numbers over the

6 papyrus or reed x rocky shore or rocks sand/rocky bottom trough Fig. 2. Main sampling area of HEST in the northern part of the Mwanza Gulf. Stations BB and A to K were sampling points on the research transect. Rock habitats were sampled among others at Anchor Island, Nyegezi Rocks, Hippo Island, Saa nane Island and Nyamatala Island.

7 7 Table 2. Number of haplochromine species per trophic group caught between 1979 and 1982, at stations on a transect across the Mwanza Gulf. Catches were made by bottom trawl and at stations E and G also by surface trawl. Species which were only obtained by surface trawl are represented separately preceded by + (n = number of bottom trawl samples, n+ = number of surface trawl samples). Means are only given for bottom trawl catches. Stations Depth in m Trophic group A/B 2-6 n= 16 C/D 2-6 n= 16 E 7-8 n= 28 n+= 8 F n= 18 G 1-14 n= 29 n+= 8 H 1-14 n= 10 I n= 9 J 7-8 n= 10 K 4 n= 7 Total. detritiv./phytopl phytoplanktivores epilithic alg. gr epiphytic alg. gr phar. moll. crush oral. moll. shell zooplanktivores insectivores prawn eaters piscivores s.s paedophages scale eater parasite eaters unknown Total Mean s.d. ±.7 ±.2 ± 2.7 ± 2.9 ± 2.7 ± 2.4 ± 2.8 ±.9 ± 2.0 Table. Number of haplochromine species per trophic group caught between 1978 and 1979 and in 1990 along rocky shores in the Mwanza Gulf. Most catches were made by angling. Additional catches were made with traps in 1979 and with gill nets in Only species for which rocks are a main habitat are included (see Appendix ; n = number of catches). Trophic group epilithic algae scrapers pharyngeal mollusc crushers oral mollusc shellers zooplanktivores insectivores piscivores s.s. paedophages crab eater unknown Total Year n= n= 78 various habitats along the transect is summarized below : (1) Sub-littoral mud bottoms (stations E to J, depth range 7-14 m (Fig. 2). The total number of species collected with the small bottom trawler ranged from 29 to 47 (Table 2). Surface trawl samples at station E and G revealed in addition seven and four species, respectively. The lower number of species collected with the small bottom trawl over the mud stations H to J is probably a sampling artifact, a result of the lower number of samples at these stations. This is corroborated by Fig. where cumulative numbers of species are given for the neighbouring stations G and H of the same depth. Only after taking 20 samples does the curve describing the number of species start to level off. The mean number of species per sample was not different among the sub-littoral stations (Table 2). (2) Littoral mud bottoms (stations C/D and K, depth range 2-6 m). At station C/D, 4 species

8 Composition of trophic groups along the transect prior to the decline U Q) a) E Z Number of samples Fig.. Cumulative number of species caught with the small bottom trawl in the period 1979 to 1982 at station G and station H (1-14m deep). were caught, at station K only 28 (Table 2). The difference is probably a result of the low number of samples taken at the latter station. The mean number of species per sample at both stations did not differ significantly (Table 2). At station C/D the mean number was slightly higher than at each of the deeper mud stations E to I (Mann-Whitney U Test, p < 0.05). ( ) Littoral sand bottom (station A/B, depth 2-6 m). Compared to the other stations, the exposed sandy littoral habitat in Butimba Bay harboured the highest number (65) of species (Table 2). The mean number of species per standard sample at the shallow sand station A/B was distinctly higher than at the mud stations (Table 2 ; Mann- Whitney U Test, p < 0.001). Greenwood (1974) also reported a higher number ( 5) of haplochromine species at an exposed sandy beach than at a sheltered bay with a mud bottom (21 species). (4) Rocky shores. Along the rocky shores, 1+ species were caught (Appendix, Table ; van Oijen et al. 1981). Eleven of these were restricted to rocks. For eight additional species, rocky shores were one of the main habitats, while the remaining species were occasional intruders in this habitat. The number of species differed considerably among trophic groups along the transect (Table 2) and partly reflects the estimated lake-wide species diversity among these groups (Table 1). The piscivores sensu stricto outnumbered all other groups. Phytoplanktivores, algae grazers, prawn eaters, parasite eaters and scale eaters were represented by few species in the trawl catches ; plant eaters and the crab eater were absent. The prawn eaters generally occurred in water deeper than 15 m ; only two of the 1 + species in the lake were caught on the transect. Plant eaters, feeding on phanerogam tissue, and epiphytic algae grazers were mainly found close to the shore in the immediate vicinity of submerged vegetation. Although the principal habitat of these groups could not be sampled with the trawler, a few species of the latter group were caught in trawls at the shallow stations (A/B, J and K ; Table 2, Appendix 1). Epilithic algae grazers and the crab eater were restricted to rocky shores (Table, Appendix ). Only once was an individual of an epilithic algae grazer caught with the trawl (Table 2, Appendix 1). Oral shelling molluscivores and insectivores were mainly associated with the sandy habitat (Appendix 1). Individual species within trophic groups usually had different spatial distributions (Appendix 1, 2, ). Important abiotic factors correlating with distributions included bottom type, water depth and exposure to wind (Greenwood 1974, 1981, van Oijen et al. 1981, van Oijen 1982, Witte 1981, 1984b, Hoogerhoud et al. 198, Goldschmidt et al. 1990, Goldschmidt & Witte 1990). The abundance of species and trophic groups differed strongly between stations. Forty six of the total of 110 species were so common that they occurred in at least 50% of the trawl catches at one or more stations (Appendix 1, 2). The bulk of the catches over sub-littoral mud bottoms was composed of detritivores/phytoplanktivores. The zooplanktivores were the second most abundant group in this habitat. Together these two groups constituted more than 90% of the number of haplochromines in the catches at stations E to J (Table 4, 5 ;

9 9 Table 4. Number (and percentage) of haplochromines per trophic group in bottom trawls of 10 minutes duration at station E. n = number of catches used for calculating mean number and percentage respectively ; detr./phytopl. = detritivores/phytoplanktivores. Trophic group 1979/80 (n = 1, 18) mean ± s.d. 1981/82 (n = 9, 10) 1987/88 (n = 9) mean ± s.d. mean ± s.d. detr./phytopl ± ± ± 0. (77.1%) (75.2%) zooplanktivores 87.7 ± ± ± 0. (18. %) (22.6%) insectivores 2.9 ± ± (1.9%) (0.4%) molluscivores 14.7 ± ± (0.5%) (0.2%) piscivores 2.6 ± ± 7. 0 (0.9%) (0.6%) other 2.6 ± ± (1.2%) (1.0%) Total ± ± ± 0.7 Witte 1981). However, insectivores dominated at the shallow stations A/B and C/D. This group constituted ca. 70% of the catch at station A/B with a sandy substratum (Witte 1981). Most piscivorous species as well as the parasite eating species were caught infrequently (Appendix 1, 2) and in low numbers. Decline of haplochromines as a group Since the start of the trawl fishery on haplochromines in the Mwanza Gulf in 197, catch rates have shown an almost continuous decline (Fig. 4). In the first four years catches of haplochromines with a 90 mm codend decreased from ca. eight to less than one kg h - '. With this codend only large (> ca. 17 cm SL) haplochromines were retained. From Table 5. Number (and percentage) of haplochromines per trophic group in bottom trawls of 10 minutes duration at station G. n = number of catches used for calculating mean number and percentage respectively ; detr./phytopl. = detritivores/phytoplanktivores. Trophic group 1979/80 (n = 1, 18) mean ± s.d. 1981/82 (n = 10, 11) mean ± s.d. 198 /84 (n = 17) mean ± s.d. 1985/86 (n = 4) mean ± s.d. 1987/88 (n = 9) mean ± s.d. detr./phytopl ± ± ± ± (85.2%) (78.9%) (82.2%) (2.1%) zooplanktivores 15.1 ± ± ± ± ± 0.7 (8.7%) (16.4%) (16.9%) (76.8%) insectivores 25.6 ± ± ± (.1%) (.1%) (0.7%) molluscivores 5.4 ± ± ± (0.4%) (0.2%) (0.1%) piscivores.5 ± ± ± (0.2%) (0.2%) (0.1%) other 2.8 ± ± ± (2.4%) (1.1%) (0.1%) Total ± ± ± ±

10 Haplochromines n = Station E a 20 mm codend mm codend n ~~ ~"4-~~4-a- L Y Nile perch 0 20 mm codend 0 90 mm codend 0 0 L 50.) c-q_~' ~ '72 '74 '76 '78 '80 '82 '84 '86 Year 0 Fig. 4. Mean catch rates of haplochromines (above) and Nile perch (below) in bottom trawl catches of R.V. Mdiria made in the Mwanza Gulf. 198 on Nile perch catches increased strongly in the Mwanza Gulf (Fig. 4). Between 1979 and 1988 catch rates of haplochromines along the transect decreased dramatically. Mean catch rates per 10 min at stations E and G decreased from 2 00 and 1 00 fishes, respectively, to virtually zero (Fig. 5, Table 4, 5). The decline in catch rates apparently began in 1981/1982 or earlier. Trawl catches in deep water, north of Kome Island, also showed a strong decline between 1984 and 1986 (Fig. 6). Thirteen catches in 1986 did not yield a single kilogram of haplochromines. In the period 1987 to 1989, 45 trawl shots were made in the Kagera area (40-50m deep) ; no haplochromines were caught on these occasions. In the same Fig. 5. Mean number (and one standard deviation) of haplochromine fishes in catches of 10 minutes with the small bottom trawl. area the mean catch rate had been 0 kg h - t in 1985 (Goudswaard personal observations). Kudhongania & Cordone (1974) reported average haplochromine catch rates of 400 to 500 kg h -1 at the beginning of the 1970s in the 40 to 60 m depth zone. Decline in species number The number of haplochromine species encountered in bottom trawl samples on the transect decreased from 1979 onwards (Fig. 7, Table 6, 7). The number of samples was always less than 20, which

11 a n=7 5 - n=18 n=10 Station E a 0 - O N o 15 E z n=9 so- 1979/ / / / / n= n=18 Station G n= N m Year E 15 n = 19 ONE Fig. 6. Mean catch rate (and one standard deviation) of haplochromine fishes in bottom trawl catches of R.V. Kiboko made in deep water, north of Kome Island. Nile perch were already abundant in this area when the trawl survey started in Z / /82 n=9 198 / / /88 Year seemed to be the minimum number of standard samples required to catch the maximum number of species (cf. Fig. ). Therefore, the apparent decrease in 1981/1982 may be spurious. However, the decrease in 198 /1984 (Fig. 7) cannot be ascribed to a lower number of samples, since a slightly higher number of samples was examined (n = 19 vs. 18). The number of species per sample at station G decreased significantly in the course of time for each trophic group (Spearman rank correlation, p < 0.01 for all cases). Until 1984 it was especially the piscivorous species that began to be found less frequently in the catches (Fig. 7, Table 6, 7). Between 1984 and 1987/1988 species belonging to other trophic groups also rapidly disappeared from the catches. In 1987/1988 only one zooplanktivorous and one detritivorous/phytoplanktivorous species (each represented by only a single individual!) were caught with the bottom trawl at station E and only one zooplanktivorous species (represented by three individuals) was caught at station G (Table 8). %///r, Rest Pisciv. Mollusc. Zoopl. Q Insect. Detr./phyt. Fig. 7. Numbers of haplochromine species per trophic group in standard samples (in 1987/88 total catch) from catches with a small bottom trawl. Detr./phyt = detrivores/phytoplanktivores ; Zoopl. = zooplanktivores ; Insect. = insectivores ; Mollusc. = molluscivores ; Pisciv. = piscivores ; Rest = remaining trophic groups and species of which the diet is unknown. Present situation along the transect and on the rocky shores Results of bottom trawl samples on the transect in 1987/1988 and in November 1990 are given in Table 8. Only six or seven species were present in these catches : the zooplanktivorous H. laparogramma, H. pyrrhocephalus and H. 'argens', the detritivorous/phytoplanktivorous H. 'morsei' and two or three unidentifiable species. At the majority of the stations however, only a few samples were taken. A more reliable impression of the present situation and the decrease in species richness since 1982 at different depths on the transect is shown in Figure 8. For the period 1987 to 1990 every catch was included, irrespective of gear type. During this

12 12 Table 6. Number of haplochromine species per trophic group in bottom trawl catches at station E. n = number of catches ; detr./ phytopl. = detritivores/phytoplanktivores. Trophic group 1979/80 (n = 18) total (mean ± s.d.) 1981/82 (n = 10) total (mean ± s.d.) 1987/88 (n = 9) total (mean ± ( s.d.) detr./phytopl (4.4 ± 0.8) (4. ± 0.6) (0.1 ± 0. ) zooplanktivores (.1 ± 1.0) (.7 ± 1.4) (0.1 ± 0. ) insectivores (1.4 ± 0.9) (1.2 ± 1.1) molluscivores (1.6 ± 0.7) (0.8 ± 1.0) piscivores (1.5 ± 0.8) (1.4 ± 1.0) other (0.1 ± 0. ) (0.2 ± 0.4) Total 5 2 (12.1 ± 2. ) (11.6 ±.2) (0.2 ± 0.7) period 79 catches (12 bottom trawls, 49 surface trawls and 18 gill net sessions) at station G and surroundings (1-15m) revealed only seven individuals of H. laparogramma, two of H. pyrrhocephalus and one unidentifiable individual. In shallower water (< 8 m ; stations BB, A/B, C/D and E) ca. 0% of the species were still caught in 1987/ This is considerably more than the percentage of species that was still present in the bottom trawls during the day (cf. Fig. 7a, Table 8). The additional species were obtained mainly with gill nets, both during day and night ; the catches were always small, particularly at station E. In the littoral zone (2-6 m) haplochromines were only caught Table 7. Number of haplochromine species per trophic group in bottom trawl catches at station G. n = number of catches ; detr./phytopl. = detritivores/phytoplanktivores. Trophic group 1979/80 (n = 18) total (mean ± sd) 1981/82 (n = 11) total (mean ± sd) 198 /84 (n = 19) total (mean ± sd) 1985/86 (n = 4) total (mean ± sd) 1987/88 (n = 9) total (mean ± sd) detr./phytopl (4.6 ± 1.1) (4.6 ± 1.6) (. ± 1.0) (1.5 ± 1.0) zooplanktivores (4. ± 1.6) (4.1 ± 2.0) (4.4 ± 1.4) (.0 ± 0.0) (0.1 ± 0. ) insectivores (1.2 ± 0.5) (1.5 ± 0.7) (0.8 ± 0.8) molluscivores (0.6 ± 0.6) (0.5 ± 0.5) (0.2 ± 0.4) piscivores (1.1 ± 1.2) (1.2 ± 0.7) (0.2 ± 0.4) other (0.7 ± 0.7) (0.6 ± 0.8) (1.1 ± 0.2) Total (12.4 ±.0) (12.5 ± 2.2) (10.1 ± 2.8) (4.5 ± 1.0) (0.1 ± 0. )

13 1 with gill nets at station BB and not with the bottom trawl at stations A/B and C/D. This suggests that these fishes mainly stayed in the shallowest parts of the Butimba Bay. The oral shelling molluscivores, the epiphytic algae grazers and the insectivores were the least affected trophic groups in the littoral zone (Fig. 8, Appendix 1). Species diversity on rocky shores also decreased (Table ). It was particularly the occasional intruders and the species that were not strictly confined to rocky shores that had vanished in 1990 (Appendix ). All species which, in 1978/1979, were regarded as occasional intruders into the habitat disappeared from the catches. Of these, H. 'kribensis', Macropleurodus bicolor, H. 'argens', H. piceatus and H. `thick skin' were still (occasionally) caught in other habitats in 1987/1990 (Appendix 1). Of the eight species of which rocky shores were one of the main habitats in 1978/1979, four were no longer present in These species were the piscivore H. 'guiarti-like', the paedophages H. melanopterus and H. barbarae, and the zooplanktivore H. `double stripe'. A fifth species, H. `grey Table 8. Number of haplochromines caught between 1987 and 1990 in bottom trawls during the day at stations along the transect (trawling time = 10 min in 1987 and in 1990, 15 min in 1988 with the exception of A/B and C/D, always 5 min). Stations A/B C/D E F G H I J Mar Apr pyr - 2 lap det May Jul flap 0 Dec flap 5 lap lap 0 Jan arg 0 Feb Jun Oct Nov mor 0 1 pyr 5 juv arg = H. argens (zooplanktivore) ; det = detritivore/phytoplanktivore ; juv = juveniles (unknown) ; lap = H. laparogramma (zooplanktivore) ; mor = H. 'morsei' (detritivore/phytoplanktivore) ; pyr = H. pyrrhocephalus (zooplanktivore) ; -_ not sampled. N ay a E 1979/ / / /1990 Year /,/ Rest ~d Mollusc. /[ A Zoopl. Algae Pisciv. = Insect. Detr./phyt. 1979/ /1990 Fig. 8. Total number of haplochromine species in and at three different depth ranges along the transect. Numbers of samples from the small bottom trawl (BT), the surface trawl (ST) and gill nets (GN) on which the figures are based are : 2-6m /1982, 1ST ; 1987/1990, 9BT, 18GN ; 7-8 m /1982, 18BT, 8ST ; 1987/1990, 12BT, 8ST, 18GN ; 1-15 m /1982, 18BT, 8ST ; 1987/1990, 12BT, 49ST, 18GN (see also material and techniques). Algae = epiphytic algae grazers ; see Fig. 7 for other abbreviations. pseudo-nigricans' (food unknown) declined and may have also disappeared.' The catch frequency of the insectivore H. chilotes and the oral shelling molluscivore H. sauvagei, which are not confined to rocks, decreased. Of the eleven species restricted to the rocks, the crab eater H. `smoke' was no longer present in the catches in 1990, while the insectivore H. `rock-picker' declined and probably vanished.' The catch frequency of the epilithic algae grazer H. 'kruising', the insectivore H. 'pseudo-rock-picker' and H. `purple rocker' (food unknown) also decreased. In contrast to what has been previously published (Anonymous 1991) the a Due to identification problems we are not completely sure that no individuals of this species were caught.

14 14 catches of the zooplanktivorous H. nyererei did not decline. This species seems to flourish at present and at certain localities the maximum size of individuals has increased by one to two centimetres (Bouton & Witte personal observations, O. Seehausen personal communication). Two species of the group restricted to rocks were caught more frequently than previously : the pharyngeal mollusc crusher H. `stone' and the insectivore H. `black pseudo-nigricans'. The pharyngeal mollusc crusher Astatoreochromis alluaudi is the only species which was caught several times near the rocks in 1990, while previously it had not been recorded in such catches. It also still occurred in other littoral areas of the lake (Bouton personal observations, O. Seehausen & L. Kaufman personal communication). This non-endemic haplochromine species does not seem to be confined to any particular type of substratum (Greenwood 1959). Discussion Controversy about the decline of haplochromine species Our monitoring of a transect across the Mwanza Gulf over 9 years clearly depicts how drastic the decline of haplochromines has been. This decline was found not only at the transect, but also for the whole Mwanza Gulf and all other areas which were monitored (e.g. Emin Pasha Gulf, Speke Gulf, Kagera area) in the Tanzanian part of Lake Victoria (Goudswaard personal observations). These results confirm earlier reports on the decline of the haplochromines in Lake Victoria (Arunga 1981, Okemwa 1981, 1984, Hughes 198, 1986, Barel et al. 1985, Goudswaard & Witte 1985, Okaronon et al. 1985, Goudswaard 1988, Goudswaard & Ligtvoet 1988, Ogutu-Ohwayo 1990a, 1990b, 1990c). However, several authors (Seegers 1987, Anonymous 1987, 1988, Harrison et al. 1989) argue that the seriousness of the situation has been exaggerated. The latter three refer, among others, to a combined expedition of HEST and the Natural History Museum (London) in It is true that many species were collected in a variety of habitats during this expedition. However, no conclusions on the decline of the haplochromines can be drawn from these data since sampling was not random. On the contrary, those areas were selected (e.g. Emin Pasha Gulf) which during that period were known to still possess a remnant haplochromine fauna. Moreover, these critics (Seegers 1987, Anonymous 1987, 1988, Harrison et al. 1989) made no comparison with the haplochromine communities before the arrival of the Nile perch. In the Emin Pasha Gulf, from which `large catches' of haplochromines were reported in 1986 by Harrison et al. (op. cit.), catch rates had already changed considerably since In June 1985 the mean trawl catch rates for haplochromines and Nile perch were 22 ± 2 5 and 54 ± 82 kg h - ' (n = 9), respectively. In August 1986 catch rates had dropped to 64 ± 115 kg h - ' for haplochromines while Nile perch catches had increased to 107 ± 89 kg h -1 (n = 11) (Goudswaard & Ligtvoet 1988). Authors (Seegers op. cit., Anonymous op. cit., Harrison et al. op. cit.) who were sceptical about the seriousness of the decline mentioned that haplochromines were common in inshore areas. This is indeed corroborated by our findings. However, in spite of the relative abundance of haplochromines in the littoral region, our data clearly demonstrate that a considerable decrease of species has occurred in this region too. Overall, there has been a significant decrease of haplochromines lake-wide. The impact of fisheries and the Nile perch on the haplochromine stock In several publications (e.g. in Barel 1986, Acere 1988, Anonymous 1988, Harrison et al. 1989) it has been suggested that the Nile perch is only partly to blame for the decline of the haplochromines during recent years ; another important cause being overfishing. In inshore areas of the Winam (= Nyanza = Kavirondo) Gulf where fishing is banned, haplochromine catches were considerably larger than in neighbouring areas where fishing is allowed (Anonymous 1988, Harrison et al. 1989). We agree that fishing has had deleterious effects on haplochromines (Marten 1979, Witte 1981, Witte &

15 15 Goudswaard 1985, Goudswaard 1988). The decline of the catch rates in the sub-littoral areas of the Mwanza Gulf (Fig. 4) was initially the result of the trawl fishery which started in the 1970s on the unexploited stocks in this area. At the beginning of the 1980s, particularly from 198 on (Fig. 4), rapidly increasing predation by Nile perch on the haplochromines was added to this fishing pressure. Consequently, it is difficult to separate the effects of fishing and Nile perch predation in the sublittoral area of the Mwanza Gulf in the 1980s. However, even in areas without fishing pressure, like the deepwater station north of Kome Island, haplochromines disappeared rapidly (Fig. 6). Nile perch were already abundant in these areas when the trawl surveys started in 1984/1985 (Goudswaard & Witte 1985, Goudswaard & Ligtvoet 1988). In the littoral habitats of Butimba Bay (stations A/B, C/D and BB ; Fig. 2) virtually no fishing occurred except for our own sampling program ; from 1981 to 1987 there was no sampling in this area. In spite of this, a dramatic decrease in species number was observed (Fig. 8, 2-6 m). There is a remarkable coincidence of Nile perch increase and haplochromine decline in various areas of Lake Victoria. In the Winam Gulf the Nile perch boom started in 1978/1979, while simultaneously haplochromines disappeared from the catches (Arunga 1981, Okemwa 1981, Hughes 198 ). The upsurge of the Nile perch in the eastern part of the Tanzanian waters (e.g. near Ukerewe and in the Speke Gulf) occurred later than in the Winam Gulf. Large Nile perch catches (average 200 kg h- ') and low haplochromine catches in the eastern part were not observed before the end of 198 (Goudswaard & Witte 1985). The mean catch rate of Nile perch in the lightly fished south west corner of the lake (Emin Pasha Gulf) was still low (54 kg h - ') in June However, Nile perch catch rates in this area doubled during the period 1985 to 1986 (see above), while haplochromine catches declined strongly (by ca. 80%). We conclude that the impact of Nile perch predation on haplochromines has been much greater than that of fishing. High fishing pressure on haplochromines existed only locally in the littoral and sub-littoral zone (e.g. near densely populated areas) ; Nile perch, on the contrary, occurs lakewide. The fishery never resulted in the complete eradication of a haplochromine community in any habitat, though it did cause the local disappearance of individual species (Marten 1979, Witte & Goudswaard 1985, Goudswaard 1988). However, the Nile perch boom coincided with the disappearance of complete haplochromine communities, even in areas where fishing pressure was absent. Stomach content analyses revealed that haplochromine cichlids were indeed the main prey of Nile perch until the former had been virtually eradicated (Gee 1969, Okemwa 1981, Hughes 1986, Ogari & Dadzie 1988, Ligtvoet & Mkumbo 1990, Ogutu-Ohwayo 1990c). Estimate of the total decline in haplochromine species diversity Although we cannot prove that the species which vanished from the areas monitored by HEST have disappeared in other parts of the lake as well, the ubiquity of the Nile perch makes this highly probable. On the transect and in the neighbouring rock habitats, more than 80 (ca. 70%) of the 12 species that were originally present have now disappeared (Appendix 1, 2, ). A rough calculation based on the decline in this area suggests that lake-wide about 200 endemic cichlid species have already disappeared or are threatened with extinction. Indeed this estimate is conservative ; original species diversity on the transect was underestimated because only data of the small trawler were used. According to our estimate ca. 100 haplochromine species should be still present in the lake. This estimate may be increased when some of the littoral habitats (e.g. the papyrus fringes and rocky shores) are studied more thoroughly. Indeed, some new species were found recently along the rocky shores (Bouton personal observations, O. Seehausen personal communication). Further, at least one new species has been repeatedly located in scattered, sub-littoral refugia on soft sediments near the mouth of the Winam Gulf (Lake Victoria Research Team, L. Kaufman personal communication).

16 16 Differential sensitivity to extinction among trophic groups Our data suggest that some species were more prone to extinction than others. Many of the piscivorous species were the first to disappear from the catches (Fig. 7b, Table 7). On the other hand, several zooplanktivorous species disappeared at the lowest rate from the catches in the sub-littoral region (Table 5, 7, 8 ; Wanink 1991). These differences may have been related to the abundances of the species, their adult sizes and the habitats where they lived. Species belonging to a particular trophic group often had similar size ranges and macrohabitat preferences (Witte & van Oijen 1990). Therefore, differences in the rate of disappearance were observed among trophic groups. Abundance All other things being equal, rare species are more susceptible to extinction than abundant species (Vermeij 1986). In early surveys the most abundant species were found among the detritivores/phytoplanktivores and zooplanktivores, while most piscivorous and molluscivorous species were relatively rare. Insectivores were more abundant than piscivores and molluscivores. As discussed below, there are indications that indeed rare species disappeared earlier than abundant species. However, as many of the rare species are also physically larger, the effects of abundance and size are not always easy to separate. Size Most piscivores were relatively large (> 10 cm SL) compared to detritivores/phytoplanktivores and zooplanktivores (5-9 cm SL) (Fryer & Iles 1972, Greenwood 1981, Witte & van Oijen 1990). The molluscivores and insectivores were intermediate in size, the latter group containing more small species than the former. Most fishing gear used in Lake Victoria was selective for larger haplochromines. This is also evident from the rapid decline of the haplochromine catches with a 90 mm codend mesh, in the first years after the onset of the trawl fishery in the Mwanza Gulf (Fig. 4). The catch frequency of two relatively rare and large paedophagous species (H. microdon and H. `black cryptodon') decreased significantly between 1978 and 1982 (Witte & Goudswaard 1985). H. 'ursus', a large and rare oral shelling molluscivore of the sub-littoral habitat, was not caught anymore after 198 (erroneously recorded as 1982 in Goudswaard 1988). A similar decrease of large species as a result of fishing with small meshes was observed for the haplochromine cichlids in the Winam Gulf (Marten 1979) and for demersal cichlid stocks in Lake Malawi (Turner 1977a, 1977b). It is not clear whether Nile perch select for large prey ; it has been described as a non-selective predator (Hamblyn 1966, Gee 1969, Ogari 1985, Ogari & Dadzie 1988). However, in these studies, no quantitative comparisons were made between prey size distributions in the environment and in the distributions observed in stomach contents. Besides a decrease of large species, a decrease in mean (and maximum) size of many small zooplanktivorous and detritivorous species was observed, especially after the upsurge of the Nile perch (Witte & Goudswaard 1985, Witte & Witte-Maas 1987, Goldschmidt & Witte 1990, Witte et al. 1990). However, there are indications that this decrease may be due to a retarded growth rate rather than to selective fishing or predation (Witte & Witte-Maas 1987). Surviving zooplanktivorous species increased again in size after 1986 in the presence of Nile perch (Wanink 1991). Habitat overlap A third factor determining the rate of extinction is habitat overlap with Nile perch. Witte & Goudswaard (1985) predicted that pelagic zooplanktivorous and phytoplanktivorous haplochromines might be less seriously affected by the more demersal Nile perch than benthic haplochromines. However, zooplanktivores in the sub-littoral area of the Mwanza Gulf showed a dramatic decline in absolute catch rate, just like other trophic groups. In spite of this, some support for the hypothesis was found since the percentage of zooplanktivores within the haplochromine catches increased strongly (Table 5, 8 ; Wanink 1991). Apparently the zooplanktivores decreased at a slower rate than the

17 17 benthic detritivores/phytoplanktivores. Of the much rarer pelagic phytoplanktivores only H. 'kribensis' was still caught in 1987/1990 (Appendix 1, 2). Like reduced vertical overlap, reduced overlap in horizontal distributions may explain the survival of certain species. Indeed, in 1987/1990 the largest numbers of haplochromine species were found in the littoral areas (Fig. 8, Table ) where the larger, piscivorous Nile perches were either relatively rare or absent (Ogari 1985, Goudswaard & Ligtvoet 1988, personal observations). Similar observations have been made in Lake Kyoga ; haplochromine species which were abundant before the Nile perch introduction became rare with relict populations being restricted either inshore or to areas of aquatic macrophytes (Ogutu-Ohwayo 1985, 1990b). In the littoral habitat, molluscivores and insectivores were less seriously affected than other trophic groups (Fig. 8), in spite of the fact that these species are larger and less abundant than the zooplanktivorous and the detritivorous/phytoplanktivorous species. Most of the molluscivorous and insectivorous species are fulltime residents in the littoral habitat. This explains why these species were least affected by the Nile perch. In contrast to this, many zooplanktivores, detritivores/phytoplanktivores and piscivores mainly occurred outside the littoral area. They used the littoral habitat either as a nursery area (e.g. H. 'nigrofasciatus', H. piceatus, H. argenteus, H. plagiostoma, H. pyrrhopteryx, H. bareli, H. microdon, H. welcommei, see Witte 1981, Goldschmidt et al. 1990, Witte & van Oijen 1990, van Oijen 1991) or as a brooding area (H. 'argens', see Goldschmidt & Witte 1990). Some of these species appeared to be occasional intruders, occurring infrequently in the littoral habitat (Appendix 1) and/or in small numbers (H. cinctus, H. `dusky wine-red fin', H. heusinkveldi, H. laparogramma). Although the Nile perch had been caught in the vicinity of rocky shores, it was not caught between the rocks. This could explain why most stenotopic rock-dwellers survived in contrast to occasional intruders (Appendix ). Of the eight species that were not restricted to the rocky habitat, four or five had disappeared. It is not known why these species did not survive near the rocks. Two possibilities are that (1) they only occurred at the periphery of the rocky habitat -(this certainly held for H. 'guiartilike') and were within the reach of Nile perch and (2) they migrated to a Nile perch-frequented habitat at certain stages in their life cycle. The crabeater H. `smoke' and the insectivore H. 'rockpicker' were the only permanent rock dwellers which were no longer present in We have no explicit explanation for their extermination. However, changes in the fish communities and the food web as a result of the Nile perch boom (see below) may have influenced species in ways other than by direct predation. Observations in the northern (Ugandan) part of Lake Victoria confirm the foregoing results. The haplochromines which are still present belong mainly to the rock-dwelling species, to the species inhabiting the inshore areas close to vegetation and to the pelagic zooplanktivores (Ogutu-Ohwayo 1990b, O. Seehausen personal communication, S.B. Wandera personal communication). Differential sensitivity to extinction among piscivores To test the hypothesis that abundance, body size and habitat overlap with the Nile perch are important factors in determining the rate of extinction we examined one trophic group more thoroughly. The piscivores showed interspecific differences in abundance (although not extreme). They showed a wide range in body size and occupied different habitats. We predicted that small and abundant piscivores and/or piscivores with a reduced habitat overlap with Nile perch would disappear later than others. Some evidence for this has indeed been found. H. `micro-obesus' was the only piscivorous species which was still caught at station G in 198 /1984 (in four of the 19 catches, Fig. 7b, Table 7). This small species (6-8 cm SL), which belonged to the subgroup of the paedophages, used to be one of the two most frequently caught piscivores at this station (Appendix 1). The other common species, H. plagiostoma, a piscivore sensu stricto, had an adult size of cm SL. This larger species was even

18 18 more numerous than H. 'micro-obesus', but it was no longer caught in 198 /1984. In 1978 five tows with a large trawler in the northern part of the Mwanza Gulf (Fig. 2) yielded 29 species of haplochromine piscivores sensu stricto of various sizes ( small, < 9 cm SL ; 21 intermediate, 9-18 cm SL ; 5 large, > 18 cm SL). Two of these species were partly pelagic and the remainder benthic. A similar effort in this area in 1985 yielded only three piscivorous fishes. One was an individual of the small (ca. 8 cm SL) and relatively common (Appendix 1) H. perrieri ; the other two were individuals of the two species of intermediate size which were pelagic. The only piscivores that were still caught 1987/ 1990 were an unidentified species near the rocks (Appendix ) and H. percoides (Appendix 1). This small species (ca. 9 cm SL ; Greenwood 1962) is the only piscivore known to be restricted to water shallower than m (van Oijen 1982). These observations support the idea that abundance, size and habitat overlap are indeed important factors in determining rates of extinction. Changes in the food web and the fish harvest The food web of Lake Victoria, especially that of the sub-littoral and deepwater regions, changed considerably due to the increase of Nile perch and the disappearance of haplochromines (Ligtvoet & Witte 1991). In biomass, the major haplochromine trophic groups in the sub-littoral zones were the detritivores/phytoplanktivores and zooplanktivores which constituted more than 40% and 16% of the total demersal fish mass, respectively (Witte & van Oijen 1990). These groups seem to have been replaced (see Daan 1980) by the native detritivorous (Fryer 1960b) atyid prawn Caridina nilotica and by the native zooplanktivorous cyprinid Rastrineobola argentea (Ligtvoet & Witte 1991). In contrast to the haplochromine zooplanktivores, the pelagic R. argentea increased strongly in numbers and biomass since the Nile perch explosion (Wanink 1991). R. argentea is considered relatively r- selected in comparison to the more K-selected haplochromines, the latter being typically low fecundity organisms with extensive parental care (Goldschmidt & Goudswaard 1989, Goldschmidt & Witte 1990, Wanink 1991). Although we realize that the dichotomy of r- and K-strategies is an oversimplification (Sibly & Calow 1986), it might be this difference in reproductive styles between the zooplanktivorous haplochromines and R. argentea which caused the striking difference in ability to coexist with Nile perch (Bruton 1990, Wanink 1991). Both C. nilotica and R. argentea became important prey of the Nile perch after the decline of the haplochromines (Ogari & Dadzie 1988, Ligtvoet & Mkumbo 1990, Ogutu-Ohwayo 1990b). Beside R. argentea, the exotic tilapiine Oreochromis niloticus is the only other fish species which currently is flourishing in the presence of the Nile perch. Oreochromis niloticus replaced the endemic tilapias and occurs in the littoral and sublittoral regions of the lake. Particularly the juveniles, which live in very shallow areas, have a minimal habitat overlap with Nile perch. These two species also coexist naturally (e.g., Lake Albert and Lake Turkana). Ligtvoet & Witte (1991) noted various characteristics in the present ecosystem which according to Rapport et al. (1985) are characteristic for ecosystems under stress : (1) decrease in diversity, (2) retrogression (a shift in species composition to organisms better adapted to overcome new and harsher environmental conditions) and ( ) changes in size composition often towards smaller mean sizes and shorter life spans. The actual catch of the fisheries in Lake Victoria increased considerably since the Nile perch boom. For many years the total annual harvest was approximately metric tons. In the second half of the 1980s this harvest rose to almost metric tons (CIFA 1988, Greboval 1990). Thus, from a fishery point of view the Nile perch could be considered successful (see Barel et al for an extensive discussion). However, as the ecosystem is still changing (see below) it is not clear whether this high harvest is sustainable. In Lake Kyoga both the total landings and the Nile perch landings have declined considerably since the extremely high

19 19 catches in the 1970s (Ogutu-Ohwayo 1990c). Currently, O. niloticus dominates the catches in this lake (Ogutu-Ohwhayo op. cit.). Prospects for the remaining haplochromines The ecosystem of Lake Victoria is currently unstable. Changes in species composition of its fauna and flora are obviously still going on. Anecdotal observations suggest increases in densities of phytoplankton, macrophytes (e.g. Ceratophyllum demersum and the exotic Eichhornia crassipes), molluscs, lake flies (chironomids and chaoborids) and oligochaetes. Such environmental changes may affect the survival of the remaining species in positive or negative ways. For example, increased occurrence of blue-green algae has been associated with deoxygenation of the hypolimnion and mass fish kills in the lake (Ochumba 1987, Ochumba & Kibaara 1989). Reappearance of haplochromines has been reported in shallow areas where the Nile perch has been reduced (CIFA 1990, Ogutu-Ohwayo 1990b). Trawl surveys in the Winam Gulf in 1988/1989 indicated an increase in haplochromine catches (from 0.0 kg h - ' to 0.4 kg h - ') at depths of three to six metres (Ogari & Asila 1990). The latest samples from the research transect in the Mwanza Gulf (a single session in summer 1991) revealed similar results. At stations E and J the number of haplochromines caught with the small trawler increased to individuals per tow (cf. Table 8) ; however, these samples contained only few species. This could mean that at least a part of the littoral haplochromine community may survive the effects of Nile perch introduction. For the sub-littoral and deepwater communities chances of a revival seem much less probable. Only for the deepwater zooplanktivore H. laparogramma are there indications that it moved to shallower water after the Nile perch upsurge (Witte & Witte-Maas 1987) where it is now one of the most abundant species (Table 8 ; L. Kaufman & O. Seehausen personal communication). Clearly, proper judgements about the conditions of the remnant haplochromine fauna can only be made if this fauna is closely monitored at the species level. The presence of Nile perch in Lake Victoria may result in the fragmentation and isolation of former haplochromine populations which might facilitate speciation. However, it seems very unlikely that speciation could balance the dramatic extinctions that have presumably occurred in this fauna. Fish species extinctions in other lacustrine environments Lakes are ephemeral habitats and frequent extinctions of fish species flocks are to be expected (Kornfield & Echelle 1984). The fossil record has documented several such extinctions, the mesozoic semionotids (McCune et al. 1984) and the pliocene sculpins (Smith & Todd 1984) being examples from North America. Two fossil cichlid flocks, each containing five types, have been described from the Oligocene and the lower Miocene (Van Couvering 1982). The cichlid species flock of Lake Victoria has not been given time to disappear naturally. Unfortunately, Lake Victoria is not unique in this respect. Lake Kyoga, which is part of the Nile system and had a fauna similar to, but much less rich than that of Lake Victoria, was stocked with Nile perch between 1954 and 1957 (Welcomme 1988). Although there is no information at the species level, the haplochromine fauna of this lake has been decimated too (Ogutu-Ohwayo 1985, 1990a, 1990b, 1990c). The Lake Lanao cyprinid flock was destroyed in less than 25 years as a result of unregulated fishing, pollution and the introduction of exotic competitors and predators (Kornfield & Carpenter 1984, Kornfield & Echelle 1984). It is believed that only three of the 18 original endemic species are still extant (Kornfield & Carpenter 1984). In Lake Atitlan (Guatamala), the largemouth bass, Micropterus salmoides, which was introduced in 1958, caused the disappearance of local fish populations (Zaret & Paine 197 ). The introduction of Oreochromis niloticus in Lake Luhondo (Ruanda) probably caused the disappear-

20 20 ance of two large cyprinid species from the lake (de Vos et al. 1990). In all of the above examples, quantitative data on the course of the changes are absent. However, such data are available for Gatun Lake which is part of the present-day Panama canal and which originated in 1910 by the damming of the Chagres River (Zaret 1979). The predator Cichla ocellaris was introduced into a tributary of the Chagres River in the 1960s (Zaret & Paine 197 ). It probably entered the lake in 1969 and moved through it `as a wave' in the following years. From 1972 onwards, the effects of C. ocellaris were carefully studied (Zaret & Paine 197, Zaret 1979, 1982). Initially, many of the effects of the introduced predator were similar to those described above for Lake Victoria. In Gatun Lake there was a reduction of more than 99% in the number of individual fishes (Zaret 1979) and a local extermination of 1 of 17 native species (Zaret 1982). However, apparently all species, except perhaps for one, have now recolonized the lake subsequent to a decline in C. ocellaris (Welcomme 1988, personal communication). The same species which were originally exterminated in the lake were able to coexist with C. ocellaris in the Chagres River (Zaret 1979, 1982). According to Zaret this difference in survival was mainly due to seasonal changes in water transparency in the Chagres River caused by the high suspended sediment loads in the rainy season. Low transparency in the rainy season resulted in a decreased feeding rate of C. ocellaris during this period. In contrast, feeding rates in the lake, which was always clear, were presumed to be consistently high. The foregoing examples of introductions of a top predator into lacustrine environments are all from the tropics. Similar observations were made in temperate zones, e.g. in northern Wisconsin lakes (U.S.A.) where the introduction of walleye, Stizostedion vitreum, and northern pike, Esox lucius, caused the decline and near extirpation of native fishes (Kempinger & Carline 1977). Apparently, fish communities in lakes are very sensitive to introductions of alien top predators. Additional examples of the effects of alien predators on native fish species can be found in Welcomme (1981, 1984, 1988) and Taylor et al. (1984). Conclusions In conclusion the following statements can be made : (1) The dramatic decline of the endemic haplochromine fauna of Lake Victoria was primarily caused by Nile perch predation, though fishing played a supplementary role in certain areas. (2) Approximately two hundred haplochromine species have already disappeared or are threatened with extinction. ( ) Large and rare haplochromine species disappeared earlier than small and abundant species. (4) Haplochromine species with a reduced habitat overlap with Nile perch disappeared more slowly than other species or, in extreme cases, were not affected. (5) Certain trophic groups (e.g. the prawn eaters and the parasite eaters) which were confined to the sub-littoral and deepwater regions may have disappeared completely. (6) The food web of Lake Victoria, especially that of the sub-littoral and deepwater regions changed considerably due to increase of the Nile perch and the disappearance of the haplochromines. (7) It is difficult to make predictions about the future status of the haplochromines in Lake Victoria as the ecosystem of the lake has not equilibrated. Remnants of the haplochromine fauna will probably survive in the littoral regions of the lake. These remnants may be threatened by high fishing pressure with small meshed nets. (8) The condition of the remaining haplochromine fauna can only be accurately judged if this fauna is closely monitored at the species level. Acknowledgements Most importantly, we are indebted to C.D.N. Barel, without whom this paper would never have been written. He initiated the Haplochromis Ecology Survey Team (HEST) in 1977 and at that time already feared that some haplochromine species

21 21 might be threatened with extinction as a result of intensive trawling. Therefore, Barel made it one of the goals of the project to collect as much biological information as possible of the then extant haplochromine community in the Mwanza area of Lake Victoria. We are grateful for his continuous and inspiring support. Over the past years many people have participated in the haplochromine research of HEST. We particularly acknowledge the contributions of R.J.C. Hoogerhoud, E.F.B. Katunzi, W. Wilhelm and M. Berger. Aloys, Mhoja and Ruben are thanked for the many years of skilful fishing. We thank C.D.N. Barel, G. Fryer, L. Kaufman, O. Seehausen and R. L. Welcomme for their valuable comments on earlier drafts of this paper. I. Kornfield kindly reviewed a later draft. M.L. Brittijn and H. Heijn drew the figures. The Tanzanian Fisheries Research Institute (TAFIRI) and the Freshwater Fisheries Training Institute at Nyegezi are acknowledged for their hospitality and support. The field work of HEST was financially supported by the Organization for the Advancement of Tropical Research (WOTRO) grants W87-129, W87-161, W87-189, W The project was also supported by the section for Research and Technology of the Netherlands Minister of Development Cooperation. References cited Acere, T.O The controversy over Nile perch, Lates niloticus, in Lake Victoria, East Africa. Naga, The ICLARM Quarterly 11 : -5. Anon The cichlid fishes of Lake Victoria - was their obituary premature? pp In: Report on the British Museum (Natural History) Trustees of the British Museum (Natural History), London. Anon Monster fish may be innocent of ecological crimes. New Scientist 1622: 4. Anon Fish's future is a bit of a mouthful. New Scientist 1756 : 20. Arunga, J.O A case study of the Lake Victoria Nile Perch Lates niloticus (Mbuta) fishery. pp In : Proceedings of the Workshop of the Kenya Marine and Fisheries Research Institute on Aquatic Resources of Kenya, July 1-19, 1981, Kenya National Academy for the Advancement of Arts and Science, Nairobi. Balon, E.K. & M.N. Bruton Introduction of alien species or why scientific advice is not heeded. Env. Biol. Fish. 16 : Barel, C.D.N The decline of Lake Victoria's cichlid species flock. Reports of the Haplochromis Ecology Survey Team 46, Zoologisch Laboratorium, University of Leiden, Leiden. 96 pp. Barel, C.D.N., R. Dorit, P.H. Greenwood, G. Fryer, N. Hughes, P.B.N. Jackson, H. Kanawabe, R.H. Lowe- McConnell, F. Witte & K. Yamaoka Destruction of fisheries in Africa's lakes. Nature 15 : Barel, C.D.N., W. Ligtvoet, T. Goldschmidt, F. Witte & P.C. Goudswaard The haplochromine cichlids in Lake Victoria : an assessment of biological and fisheries interests. pp In : M.H.A. Keenleyside (ed.) Cichlid Fishes : Behaviour, Ecology and Evolution, Chapman and Hall, London. Barel, C.D.N., M.J.P. van Oijen, F. Witte & E.L.M. Witte- Maas An introduction to the taxonomy and morphology of the haplochromine Cichlidae from Lake Victoria. Neth. J. Zool. 27 : Bruton, M.N The conservation of fishes of Lake Victoria, Africa : an ecological perspective. Env. Biol. Fish. 27 : CIFA Report of the 4th session of the sub-committee for the development and management of the fisheries in Lake Victoria. Kisumu, Kenya, 6-10 April 1987, FAO Fish. Rep. 88 : CIFA Report of the 5th session of the sub-committee for the development and management of the fisheries in Lake Victoria. Mwanza, Tanzania, September 1989, FAO Fish. Rep. 4 0 : Coulter, G.W., B.R. Allanson, M.N. Bruton, P.H. Greenwood, R.C. Hart, P.B.N. Jackson & A.J. Ribbink Unique qualities and special problems of the African Great Lakes. Env. Biol. Fish. 17 : Daan, N A review of replacement of depleted stocks by other species and the mechanisms underlying such replacement. Rapp. P.-v. Reun. Cons. Int. Explor. Mer. 177 : Fryer, G. 1960a. Concerning the proposed introduction of Nile perch into Lake Victoria. E. Afr. J. Agric. 25 : Fryer, G. 1960b. The feeding mechanism of some atyid prawns of the genus Caridina. Trans. Roy. Soc. Edinb. 64 : Fryer, G. & T.D. Iles The cichlid fishes of the great lakes of Africa. Oliver & Boyd, Edinburg. 642 pp. Gee, J. M. 1969, A comparison of certain aspects of the biology of Lates niloticus (Linne) in some East African lakes. Rev. Zool. Bot. Afr. 80 : Goldschmidt, T Egg mimics in haplochromine cichlids (Pisces, Perciformes) from Lake Victoria. Ethology 88 : Goldschmidt, T. & P.C. Goudswaard Reproductive strategies in haplochromines (Pisces : Cichlidae) of Lake Victoria. pp In : T. Goldschmidt, An Ecological and Morphological Field Study of the Haplochromine Cichlid Fishes of Lake Victoria, Ph.D. Thesis, Rijksuniversiteit Leiden, Leiden.

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