Trophic shifts in predatory catfishes following the introduction of Nile perch into Lake Victoria

Afr. J. Ecol. 1999, Volume 37, pages 457–470

Trophic shifts in predatory catfishes following theintroduction of Nile perch into Lake Victoria

J. P. OLOWO1,2 and L. J. CHAPMAN2,3

1Fisheries Research Institute, Box 343, Jinja, Uganda, 2Department of Zoology, University ofFlorida, Gainesville, Florida, 32611, U.S.A and 3Wildlife Conservation Society, 185th Streetand Southern Boulevard, Bronx, NY, 10460, U.S.A.

Summary

This study looked for evidence of trophic shifts in the diet of two predatory catfishes(Bagrus docmac and Schilbe intermedius) following the establishment of introducedNile perch (Lates niloticus) into lakes of the Lake Victoria basin. Bagrus docmacexhibited a shift from a primarily piscivorous diet dominated by haplochrominecichlids to a broader diet that included a significant proportion of invertebrates andthe cyprinid fish, Rastrineobola argentea, which became abundant following depletionof the haplochromines. Schilbe intermedius exhibited a trophic shift from a piscivorousdiet dominated by haplochromines to an insectivorous diet. The flexibility in dietexhibited by these two catfishes may have permitted these species to persist, albeitin reduced numbers, subsequent to the introduction of Nile perch and may facilitateresurgence as fishing pressure reduces numbers of large Nile perch.

Key words: Bagridae, dietary shifts, Lates, Schilbeidae, Uganda

Resume

Cette etude cherchait des preuves d’une evolution dans le regime alimentaire de deuxpoissons-chats predateurs (Bagrus docmac et Schilbe intermedius), suite a l’installationde la perche du Nil (Lates niloticus) introduite dans les lacs du bassin du Lac Victoria.Bagrus docmac presentait une evolution d’un regime au depart piscivore, domine parles cichlides haplochromines, vers un regime plus ouvert qui comprend une proportionsignificative d’invertebres et du cyprin Rastrineobola argentea, qui est devenu abondantsuite a la rarefaction des haplochromines. Schilbe intermedius a manifeste une evolutiond’un regime piscivore domine par les haplochromines vers un regime insectivore. Laflexibilite alimentaire manifestee par ces deux poissons-chats peut avoir permis a cesdeux especes de survivre, encore qu’en nombre restreint, a l’introduction de la perchedu Nil et pourrait faciliter leur recuperation alors que la pression de la peche reduitle nombre de grosses perches du Nil.

Introduction

The introduction of non-native fish species is common practice in fresh watersthroughout the world. Although fish introductions may be useful in increasing yield

Correspondence: J. P. Olowo.

1999 East African Wild Life Society.

458 J. P. Olowo and L. J. Chapman

or for biological control, they can also have many negative impacts including:predation on existing stocks, hybridization, introduction of parasites, competitionfor food with indigenous species, and the destruction or alteration of existingfood webs (Welcomme, 1984; Ogutu-Ohwayo & Hecky, 1991). Some of the mostecologically disastrous introductions have involved the transfer of predatory fishes.Impacts of large piscivores on indigenous piscivores are of particular interest, becauseintroduced predators pose a threat on different ecological dimensions. The introducedpredator may become a competitor of the native predators for preferred prey andalso a predator on smaller-sized native predators and the juveniles of the largerpredators.

One of the most well known introductions of fish predators into an aquatic systemis that of Nile perch (Lates niloticus) into Lake Victoria, the largest tropical lake inthe world (68,800 km2), with its waters shared by Uganda, Kenya and Tanzania.The establishment of Nile perch in Lake Victoria after its introduction in the 1950sled to dramatic changes in fish faunal structure and diversity. Although catches ofmany species had declined by the 1960s due to over-exploitation (Beverton, 1959),the dramatic increase in Nile perch in the 1980s was followed by a decline inpopulations of several indigenous species (Kaufman, 1992). Most notable was thedisappearance of over 50% of the 600 + species of endemic haplochromine cichlids(Kaufman, 1992; Kaufman, Chapman & Chapman, 1997). As recently as 1980,the haplochromines comprised about 84% of the fish biomass in Lake Victoria(Kudhongania & Cordone, 1974). By 1990, Nile perch comprised over 80% of thecatch, with the rest consisting mainly of Nile tilapia and the small pelagic cyprinidRastrineobola argentea.

Although much attention has focused on the mass extinction of the haplochrominecichlids, many non-cichlids also suffered declines. The most economically importantof these were the catfishes, which formed the mainstay of the fisheries beforethe introduction of Nile perch, contributing about 90,997 metric tons in stocks(Kudhongania & Cordone, 1974; Ogutu-Ohwayo, 1990a; Witte et al., 1992). At thattime, the catfishes exploited most by the artisanal fisheries were Bagrus docmac,Clarias gariepinus, Synodontis victoriae, and Schilbe intermedius (Kudhongania &Cordone, 1974; Acere, 1988). Bagrus docmac, C. gariepinus, and S. intermedius werethe top predatory fishes in Lake Victoria in the pre-Nile perch era. Bagrus docmacwas the most common and widespread catfish, well represented at all depths(Bergstrand & Cordone, 1970) and comprising approximately 6% of the fish biomass(Bergstrand & Cordone, 1970; Kudhongania & Cordone, 1974). In 1968, B. docmacaccounted for about 14% of the approximately 114,000 metric tons of fish landedby the artisanal fishery (Chilvers & Gee, 1974). Clarias gariepinus comprised ap-proximately 4% of the biomass and about 8% of the artisanal catch (Kudhongania& Cordone, 1974; Acere, 1988). The standing stock of S. intermedius was estimatedat 650 metric tons, about 0.1% of the biomass (Kudhongania & Cordone, 1974).However, the biomass of S. intermedius may have been underestimated becauseshallower areas of the lake were not adequately sampled (Goudswaard & Witte,1997). The contribution of S. intermedius to the artisanal fisheries seems to havebeen poorly documented (Goudswaard & Witte, 1997).

Commercial catch data from the areas around Napoleon Gulf in Uganda showeda decline in the biomass of B. docmac from about 29% in 1977 to about 0.01% in1989, and a decline in C. gariepinus from about 10% to about 0.16% over the same

East African Wild Life Society, Afr. J. Ecol., 37, 457–470

Trophic shifts in predatory catfishes 459

period (J. Okaronon and J. Wadanya, unpublished). This coincided with the rapidincrease in abundance of Nile perch. Data from Tanzanian waters of Lake Victoriaalso indicated a decline in B. docmac after 1984 (Acere, 1988; Goudswaard & Witte,1997). Quantitative data on changes in the relative abundance of S. intermediusduring the Nile perch upsurge are limited, but this species has not been recorded inthe Ugandan portion of the lake since the early 1980s although it has been reportedfrom some areas of Kenyan and Tanzanian waters (J. Ogari, pers. comm.; Goud-swaard & Witte, 1997).

The proposal to introduce Nile perch into Lake Victoria met with oppositionfrom fisheries biologists at the then East African Freshwater Fisheries ResearchOrganization (EAFFRO). Their main objection was that Nile perch would competewith the indigenous predators like B. docmac for their preferred prey – the haplo-chromine cichlids (Fryer, 1960; Achieng, 1990), potentially leading to decreasedsurvivorship and/or a dietary shift to alternative prey. Unfortunately, few studieshave been carried out on these species following the decline of the haplochromines,to which much of the attention has been directed. Recently, haplochromines haveshown some resurgence, and this might diminish the impact of their decline onindigenous piscivores.

The objectives of this study were to look for evidence of trophic shifts intwo predatory catfishes (Bagrus docmac and Schilbe intermedius) following theestablishment of Nile perch in lakes of the Victoria basin. To address this objectivewe compared the stomach contents of B. docmac from Lake Victoria collected atthree time periods: historical data from 1958 (Corbet, 1961) prior to the establishmentof Nile perch, 1991–92 when Nile perch catches were very high and haplochromineswere extremely rare, and 1997, a period of haplochromine resurgence. We alsocompared stomach contents of B. docmac from Lake Victoria (1991–92) to stomachcontents of B. docmac from Lake Edward, a lake without Nile perch. Schilbeintermedius could not be found in the Ugandan waters of Lake Victoria after theupsurge of Nile perch, so we compared the stomach contents of S. intermedius fromLake Nabugabo (a satellite of Lake Victoria) after the establishment of Nile perchto historical data from Lake Victoria prior to establishment of Nile perch (Graham,1929; Corbet, 1961).

Materials and methods

Study sites

The study site for our Bagrus docmac study was Napoleon Gulf, located on thenorth-western shores of Lake Victoria. The main outflow is via the River Nile, whichhas its source at the northern tip of Napoleon Gulf. The gulf averages about 10 min depth. Its northern and eastern margins are fringed by vegetation, sandy beaches,and rock; the western margin is full of rocky outcrops. Following the constructionof the Owen Falls dam across the Nile River, the water level rose and extended overpart of the river. An undercurrent exists in this part of the gulf providing loticconditions over a short section. The dam effectively cut off the lake population fromthe river.

The study site for Schilbe intermedius was Lake Nabugabo. The lake is located tothe west of Lake Victoria and is thought to have been formed when a sandbar cut



it off from the latter approximately 4000 years ago (Beadle, 1962). Lake Nabugaboaverages about 4 m in depth and is about 24 km2 in area. It is fringed by herbaceouswetland vegetation (primarily Vossia cuspidata, Miscanthidium violaceum and Cyperuspapyrus) along most of its margin, except on the western side where there are sandybeaches abutting a forested area. The papyrus-choked Juma River is the main sourceof inflow supplemented by runoff from the watershed during the rains. Outflowappears to be by underground seepage through the extensive Lwamunda Swamp(Ogutu-Ohwayo, 1993).

Nile perch were introduced into Lake Nabugabo in 1960. Before its introduction,the fisheries of Lake Nabugabo were similar to those of Lake Victoria. About 30species were recorded by the Cambridge expedition to Lake Nabugabo in 1962(CNBS, 1962; Greenwood, 1965). At that time, B. docmac, C. gariepinus and S.intermedius were the most important species for the artisanal fishery (CNBS, 1962).In 1991–92, 30 years subsequent to the introduction of Nile perch, a team of scientistsfrom the Fisheries Research Institute (Uganda) surveyed the lake and found thathaplochromines and many of the non-cichlids had become rare or had disappearedfrom the main lake (Ogutu-Ohwayo, 1993). Only one catfish, S. intermedius, remainedabundant. Since then, however, this species has gradually disappeared from the lakeand is now rare (unpublished data).

Sampling procedures

Between 1991 and 1992, while the Fisheries Research Institute of Uganda wascarrying out trawling surveys in Napoleon Gulf to study Nile perch, we tookadvantage of the trips to collect samples of Bagrus docmac, which were very rare inthe lake by this time and could not be obtained easily by gill netting or othermethods. The trawls were conducted approximately bimonthly (n=12) along twotransects. The first transect began from the source of the Nile River and ran south-westward along the western margin of the gulf. The second transect began from theend of the first transect and ran towards the north-east. Transects were repeatedtwice in opposite directions each sampling day. During the summer of 1997, samplingfor Bagrus docmac was carried out using gill nets because B. docmac had becomemore available. The nets were set deep in the lake in the same area as the firsttrawling transect. Nets were set in the evenings and retrieved the following morning.Bagrus docmac samples were obtained from Lake Edward during the summer of1996. The fish were purchased from fishermen and had been captured with gill nets.

Samples of Schilbe intermedius were obtained from Lake Nabugabo betweenOctober 1991 and August 1993 using gill nets. The nets were set in the evenings andretrieved early the next day. A few additional specimens were obtained using beachseines that were occasionally operated from sandy beaches. Attempts to obtain moresamples between 1996 and 1997 were unsuccessful because the species had largelydisappeared from the lake. Sampling in Napoleon Gulf (Lake Victoria) failed toyield any specimens of S. intermedius during the 1991–92 and 1997 sampling periods.

Biometric data including weight, length, and sex of the fish were recorded in thefield; and stomach contents were preserved in 10% formalin. In the laboratory, thestomachs were slit open and the contents spilled into a Petri dish. Prey items weresorted into categories according to the groupings used by Corbet (1961). The number



of different kinds of prey were counted, after which they were blotted dry, and theweights taken for each category to the nearest 0.01 g.

The gut contents were analysed according to the method of Hynes (1950), asreviewed by Hyslop (1980). The relative importance of different food items to a fishis best represented by using two methods in conjunction (Hynes, 1950; Hyslop,1980). In this study, the two methods used primarily were the ‘occurrence method’and the ‘main contents method’ to permit comparison with data presented by Corbet(1961). In the occurrence method, the number of stomachs containing one or moreindividuals of each prey type was recorded and expressed as a percentage of thetotal number of non-empty stomachs. In the main contents method, the number ofstomachs in which a particular prey item occupied more than 50% of the contentsof the stomach was expressed as a percentage of the total number of stomachs thatcontained food (Corbet, 1961). In addition, the weight of each category of prey inall the stomachs was expressed as a percentage of the total weight of all prey in thestomachs examined to provide an additional assessment of the importance of differentprey types.

Trophic shifts in Bagrus docmac were evaluated in two ways. First, we comparedthe importance of different prey categories between data generated by Corbet (1961)and those generated by this study during the periods 1991–92 and 1997, respectively.Second, we compared data collected from Lake Edward (1996) with the 1991–92and 1997 data from Lake Victoria. Corbet (1961) used the occurrence and maincontents method to analyse the gut contents of his specimens. For this reason, onlythe results of the occurrence and main contents method were compared with hisdata. Nevertheless, data from the percentage mass method are presented to providea more comprehensive assessment of the importance of different types of prey andchanges in diet between 1991–92 and 1997. Frequency values from Corbet’s (1961)data were converted into numbers of individuals, and new frequencies calculated forthe combined total number of fish he examined that had food. The numbers werealso used in a Chi-squared test of independence to test whether diet was independentof time period.

If piscivores shift to an invertebrate-dominated diet, foraging costs may result inloss of condition. Corbet (1961) did not report lengths and weights for individuals.However, we were able to look for a difference in the condition of B. docmac betweenour 1991–92 and 1997 samples. Condition was assessed using bilogarithmic plots ofbody length versus standard length. Analysis of covariance was used to test fordifferences in the weight-length relationships between years. For each comparison,data were tested for homogeneity of slopes before potential differences in Y-interceptswere considered (Sokal & Rohlf, 1981).

For S. intermedius, we compared the frequency of occurrence of prey types fromLake Nabugabo to data collected by Corbet (1961) on S. intermedius from LakeVictoria. The establishment of Nile perch in Lake Nabugabo was followed by fishfaunal changes similar to those that occurred in Lake Victoria (Ogutu-Ohwayo,1993). It is therefore likely that similar changes occurred in the diet of S. intermediusin the two lakes. In the absence of S. intermedius specimens from Lake Victoria,specimens from Lake Nabugabo provided an alternative source of information onthe dietary changes that might have occurred in this species in Lake Victoria. Thefrequency values from Corbet’s data were converted into numbers and comparedwith the data from Lake Nabugabo using a Chi-squared test of independence.



Fig. 1. (A) Percentage frequency of occurrence and (B) percentage main contents for different prey itemsin the stomachs of Bagrus docmac captured in Lake Victoria in 1958 (Corbet, 1961) 1991–92, and 1997.

Results

Bagrus docmac

A total of 44 stomachs of Bagrus docmac from the 1991–92 period were analysedfor gut contents. Thirty-nine of the stomachs contained food. The fish ranged insize from 23.4 to 74.2 cm standard length (SL) (mean=34.7 cm); however, onlythree fish (one female and two males) were above 50 cm SL. Frequency of occurrenceanalysis indicated odonatan larvae as the most important dietary item, followed bythe fish Rastrineobola argentea, gastropods, and the shrimp Caridina nilotica (Fig. 1a,Table 1). Nile perch occurred in 18.0% of the stomachs, whereas the frequency ofoccurrence of haplochromines was only 7.7%. Other prey consisted mainly of theephemeropteran Povilla adusta larvae, chironomid larvae and pupae, and trichopteranlarvae.

During the summer of 1997, a total of 75 fish was caught, 70 of which had foodin their stomachs. The fish ranged in size from 17.8 to 36.5 cm SL (mean=27.0 cm),and had fed mainly on gastropod molluscs, followed by Povilla adusta larvae, C.nilotica, haplochromine cichlids, and chaoborid larvae. Other prey included a varietyof invertebrates and a few fish (Fig. 1a, Table 1).



Table 1. Percentage frequency of occurrence and percentage mass of prey types in the stomachsof Bagrus docmac captured in Lake Victoria in 1958 (Corbet 1961), 1991–92 and 1997

% Frequency % Mass

Prey type 1958 1991–92 1997 1958 1991–92 1997

FishHeplochromines 57.19 7.69 30.00 – 0.85 23.29L. niloticus 0 17.95 0 – 24.45 0R. argentea 1.35 41.03 2.86 – 19.87 0.59Tilapiines 1.89 0 4.29 – 0 22.69Clarias spp. 0 0 7.14 – 0 7.12Fish remains – 30.77 20.00 – 10.05 4.11InsectsPovilla adusta (larvae) 7.46 15.39 42.86 – 0.05 6.12Povilla adusta (adults) 1.62 0 0 – 0 0Ephemeroptera (larvae) 1.26 0 0 – 0 0Ephemeroptera (adults) 0.09 0 10.00 – 0 0.08Chaoboridae (larvae) 2.16 0 27.14 – 0 0.24Chaoboridae (pupae) 0 0 15.71 – 0 0.03Chironomidae (larvae) 3.78 12.82 11.43 – 1.67 0Chironomidae (pupae) 0 12.82 15.71 – 1.25 0.04Trichoptera (larvae) 0.72 10.26 11.43 – 0.10 0.03Trichoptera (adults) 0 0 8.57 – 0 0.04Coleoptera (adults) 0 0 1.43 – 0 0.01Isoptera (adults) 0.72 2.56 4.29 – 1.41 6.61Odonata (larvae) 9.26 61.54 1.43 – 36.19 0.03Hymenoptera (adults) 0.63 2.56 0 – 0.02 0OthersC. nilotica 4.59 20.51 32.86 – 1.46 1.59Mollusca 4.59 25.64 61.43 – 0 13.98Potamon sp. 1.26 0 17.14 – 0 0Ostracoda 0.18 2.56 4.29 – 0 1.82Invertebrate remains 0 0 20.00 – 0 1.82PlantsPlant remains 4.65 0 2.86 – 0 0.20

Table 2. Percentage fre-quency of occurrence and per-centage mass of prey types inthe stomachs of Bagrus doc-mac captured in Lake Edwardin 1996

% Frequency % MassPrey type 1996 1996

FishHaplochormines 19.23 34.60Clarias spp. 3.85 26.67Fish remains 46.15 34.63InsectsChaoboridae (larvae) 23.08 0.27Chaoboridae (pupae) 23.08 2.83Chironomidae (larvae) 7.69 0.52Chironomidae (pupae) 23.08 0.21Trichoptera (larvae) 11.54 0.06Hymenoptera (adults) 3.85 0.21



Table 3. Analyses of co-variance for comparison ofthe condition factor of (a)male vs. female Bagrus doc-mac from Lake Victoria, ob-tained in 1991–92 and 1997,respectively, and (b) B. doc-mac from Lake Victoria(males and females combined)for 1991–92 versus 1997

Statistic Female Male F P

Sample period 1991–92Slope 2.920 3.136 1.416 0.241Y-intercept – 1.685 – 2.007 0.090 0.766Adjusted mean 2.805 2.811N 18 24Sample period 1997Slope 3.359 3.082 2.441 0.127Y-intercept – 2.226 – 1.871 0.060 0.808Adjusted mean 2.518 2.515N 18 21Sample period 1991–92 versus 1997Statistic 1991–2 1997 F PSlope 3.055 3.106 0.224 0.637Y-intercept – 1.883 – 1.894 32.964 <0.001Adjusted mean 2.604 2.670N 42 70

A total of 34 fish was collected from Lake Edward, of which 25 had food. Thefish ranged in size from 17.3 to 44.2 cm SL (mean=29.4 cm). Bagrus docmac fromLake Edward fed mainly on fish, primarily haplochromines (Table 2). The richnessof prey types consumed was lower for B. docmac from Lake Edward than for thosefrom Lake Victoria (Tables 1 and 2).

Diet (frequency of occurrence) was not independent of time period (v2=293.2,P < 0.001). Data obtained by Corbet (1961) showed that B. docmac 20–99 cm totallength (TL) fed mainly on haplochromines prior to the establishment of introducedNile perch (Fig. 1a, Table 1). Other prey included a variety of invertebrates and afew fish.

Analyses using the percentage main contents method revealed similar trends. InLake Victoria, the bulk contribution of fish decreased between 1958 and 1997. Thecontribution of insects increased between 1958 and 1991–92, and then dropped in1997 (Fig. 1b). Although insects occurred frequently among the stomach contentsof B. docmac obtained in 1997, their contributions in terms of bulk were smallcompared to what might be expected based on their frequency (Table 1). The decreasein the bulk of insects in the diet between 1991–92 and 1997 coincided with an increasein the importance of both Potamon spp. and molluscs (Fig. 1b).

Analyses using percentage mass could only be used to compare 1991–92 to 1997.The importance of invertebrates was smaller when using percentage mass than inthe frequency of occurrence analysis: however, the general trends (e.g. increase inhaplochromines, increase in molluscs, and decrease in R. argentea) between 1991–92and 1997 were evident.

Overall, the most notable change in the diet of B. docmac was a dramatic decreasein the importance of fish and increase in the importance of invertebrates after theestablishment and expansion of Nile perch in Lake Victoria. In addition, fish speciesconsumed differed markedly among sampling periods. The most notable shift wasa dramatic decrease in the frequency of occurrence of haplochromines from 57.2%in 1958 to 7.7% in 1991–92 when haplochromines were also rare in the main lake,and R. argentea was the main fish species consumed. This was followed by an



Fig. 2. (A) Percentage frequency of occurrence and (B) percentage main contents of different prey itemsin the stomachs of Schilbe intermedius captured in Lake Victoria in 1958 (Corbet, 1961) and in LakeNabugabo during the period 1991–93.

increase in the frequency of occurrence of haplochromines in 1997. We looked fora change in the condition of B. docmac between these last two sampling periods tosee whether an increase in the consumption of haplochromines in 1997 coincidedwith an increase in fish condition. There was no difference in condition factorbetween males and females in 1991–92 and 1997 (Table 3). The data were thereforecombined for the comparison between periods. Fish condition differed between1991–92 and 1997; B. docmac in 1991–92 weighed significantly less than fish of thesame length captured in 1997 (Table 3).

Schilbe intermedius

A total of 362 stomachs of S. intermedius from Lake Nabugabo were examinedbetween 1991 and 1993, of which 254 contained food. Individuals ranged in sizefrom 11.2 cm to 34.1 cm TL (mean=23.5 cm). Frequency of occurrence analysisindicated chironomid pupae and larvae as the most important dietary items, followedby Povilla adusta (40.6%), and chaoborid larvae (Fig. 2a, Table 4). A variety ofother invertebrates were also consumed. However, only three out of the 254 stomachsexamined contained fish.



Table 4. Percentage fre-quency of occurrence and per-centage mass of prey types inthe stomachs of Schilbe in-termedius captured in LakeVictoria in 1958, and in LakeNabugabo between 1991 and1993

% Frequency % Mass

Prey type 1958 1991–93 1958 1991–93

FishHapolochromines 27.61 0 – 0R. argentea 17.14 0 – 0Fish remains 0 4.33 – 5.95InsectsPovilla adusta (larvae) 2.86 40.55 – 40.92Povilla adusta (adults) 0.95 0 – 0Ephemeroptera (larvae) 5.24 0 – 0Ephemeroptera (adults) 0.95 0 – 0Chaoboridae (larvae) 7.62 25.98 – 1.02Chaoboridae (pupae) 0 5.51 – 0.11Chironomidae (larvae) 3.33 28.74 – 5.89Chironomidae (pupae) 12.86 48.42 – 31.21Chironomidae (adults) 3.81 0 – 0Trichoptera (adults) 0.48 0,39 – 0.01Coleoptera (adults) 0 0,39 – 0.06Isoptera (adults) 4.29 0.79 – 0.21Odonata (larvae) 2.38 4.72 – 2.26Hymenoptera (adults) 3.81 9.84 – 3.67Hemiptera (larv. & adults) 0 12.60 – 3.45OthersAnnelida 0 1.58 – 1.32Mollusca 0 1.18 – 0.96C. nilotica 4.76 0 – 0Unidentified remains 0 6.30 – 3.05PlantsPlant remains 2.38 0.39 – 0.02

Diet was not independent of time (v2=153.79, P < 0.001). Data collected in 1958(Corbet, 1961) showed that S. intermedius in Lake Victoria fed predominantly onfish at that time, mainly haplochromine cichlids and Rastrineobola argentea (Fig. 2a,Table 4). In the period 1991–93, haplochromines had become rare in both LakesVictoria and Nabugabo (Ogutu-Ohwayo, 1990a,b, 1993). The absence of haplo-chromines in the diet in 1991–93 was accompanied by a high frequency of occurrenceof various insects (Fig. 2a, Table 4).

Results from the main contents method were similar to those for the frequencyof occurrence method. The bulk contribution of fish to the diet of S. intermediuswas much higher in Lake Victoria in 1958 than in 1991–93. The contribution ofinsects was low in 1958 and much higher in the 1991–93 sample (Fig. 2b). Thepercentage mass analysis for 1991–93 showed similar trends to the frequency ofoccurrence analysis; the dominant prey by mass were chironomid pupae. Percentagemass data were not available for 1958.

Discussion

Bagrus docmac

Bagrus docmac exhibited a marked trophic shift between 1958 and 1991–92 from apredominantly piscivorous diet (mainly haplochromine cichlids) to one dominated



by invertebrates and the non-cichlid R. argentea. This dietary shift was coincidentwith the mass decline of haplochromines in the main lake. There was an increase inthe frequency of occurrence of haplochromines from 7.7% in 1991–92 to 30.0% in1997, coincident with the resurgence of some haplochromine species in Lake Victoria.A comparison among the frequency of occurrence, percentage main contents andpercentage mass in 1997 suggests that a large number of fish consumed insects, butin small numbers. Other invertebrates, primarily molluscs and Caridina nilotica weremuch more important in 1997 than in earlier samples, which may reflect the increasethat has been observed in these prey taxa in the lake. The native detritivorous prawn,Caridina nilotica, has increased dramatically over the past two decades and hasbecome one of the main prey taxa for Nile perch subsequent to the crash of thehaplochromine fauna (Ogutu-Ohwayo, 1990b). Molluscs have also increased inabundance in the lake, coincident with the loss of several mollusc-feeding haplo-chromines. Bagrus docmac from Lake Edward also fed predominantly on fish, andalthough the frequency of occurrence of the haplochromines appeared to be low,this was an underestimate because most of the unidentified fish prey appeared to becichlids (presumably haplochromines).

The fact that B. docmac from both lakes showed similar food preferences supportsthe observation by Chilvers & Gee (1974) that B. docmac is generally piscivorous.The diet of B. docmac from Lake Victoria was broader in 1997 than in 1958 andbroader than that of B. docmac in Lake Edward in 1997. This reflects a more catholictendency in the feeding behaviour of B. docmac in the presence of Nile perch. Theobserved shift to an invertebrate-dominated diet demonstrates a high degree offeeding flexibility, but the diet may be suboptimal for the species. In 1997, thefrequency of occurrence of haplochromines was much higher than in 1991–92,associated with the resurgence of some haplochromines in the main lake, and mayreflect selection for energetically optimal prey. The higher condition of fish observedin 1997 than in 1991–92 may relate to the more optimal prey base available in 1997.

Before the introduction of Nile perch, B. docmac was widely distributed in LakesVictoria, Kyoga and Nabugabo (Graham, 1929; CNBS, 1962; Chilvers & Gee, 1974;Kudhongania & Cordone, 1974). In Lake Victoria, B. docmac was found at all depths(Corbet, 1961; Greenwood, 1966) but was most abundant in 0–70 m depth range(Kudhongania & Cordone, 1974). When Nile perch became established in the lakes, itoccupied the same depth range that was occupied by B. docmac previously. It is likelythat the overlap in both diet and habitat between B. docmac and Nile perch led tocompetition on both fronts and partitioning of both diet and habitat, at least partially.

After the establishment of Nile perch, B. docmac, particularly smaller-sized in-dividuals, became confined to rocky areas around Lake Victoria and its affluentrivers. The samples used in this study were obtained in rocky areas around NapoleonGulf; however, B. docmac specimens were also frequently brought into the marketat Masese near Jinja by fishermen from the rocky outcrops of the islands within thelake. Of the 44 specimens that were caught in trawls, 33 came from the first transectthat ran along the rocky western margin of Napoleon Gulf. Most of these specimenswere relatively small compared to the ones obtained in the second transect. Theproximity of the smaller-sized B. docmac to the rocky areas suggests a protectivefunction provided by this microhabitat to size classes of B. docmac that are relativelymore vulnerable to Nile perch predation. The use of rock refugia and a shift to aninvertebrate-dominated diet may have permitted a persistence of B. docmac with



Nile perch. The complete disappearance of B. docmac in Lake Nabugabo may bedue to the fact that there are no rocky refugia in this lake. Thus, juvenile B. docmacmay have lacked adequate protection from Nile perch predation, leading to highpredation pressure on juveniles and recruitment failure.

Schilbe intermedius

Schilbe intermedius has not been caught in the Ugandan waters of Lake Victoria formany years. However, samples of S. intermedius obtained from the southern partsof Lake Victoria (K. Goudswaard, unpublished) and Lake Nabugabo (this study)suggest changes in their feeding habits and distribution that mirror those of B.docmac in Lake Victoria.

In 1958, S. intermedius from Lake Victoria fed predominantly on fish (mainlyhaplochromines). By the early 1990s data from the Nyanza Gulf of Lake Victoria(Tanzania), where S. intermedius still persists, indicated a shift to a diet dominatedby insect larvae (primarily Odonata), Rastrineobola, and young Nile perch (K.Goudswaard, unpublished). Data from the Sondu-Miriu River, a tributary of LakeVictoria (Kenya) also indicated that S. intermedius fed mainly on insects in 1990(Ochumba & Manyala, 1992). Although we were unable to sample S. intermediusfrom the Ugandan waters of Lake Victoria, the diet of fish from Lake Nabugabosuggests a shift from a predominantly piscivorous diet to an insectivorous one. It islikely that the diet of S. intermedius in Lake Nabugabo in 1991–93 reflects thedramatic decline in haplochromine abundance that followed the establishment ofintroduced Nile perch (Ogutu-Ohwayo, 1993; Chapman et al., 1996a, Chapman,Chapman & Chandler, 1996b).

Before the introduction of Nile perch into Lakes Victoria, Kyoga and Nabugabo, S.intermedius was abundant in the three lakes. In Lake Victoria, S. intermedius occupiedthe 0–60 m depth range, although it was more common in the 0–30 m range (Ku-dhongania & Cordone, 1974). Again, this was the depth range that Nile perch occupiedupon its establishment in this lake. In the eastern part of the lake, S. intermedius wasfound in shallow inshore areas and also in the affluent rivers subsequent to the dramaticincrease in Nile perch (Ochumba & Manyala, 1992); in the southern part, it was caughtin shallow inshore areas (waters less than 10 m deep) as recently as 1990 (Goudswaard& Witte, 1997). However, the apparent absence of S. intermedius in the northern partis curious and may relate to other factors like the lack of access to the affluent riversfor spawning purposes. The Nile River is now cut off by the Owen Falls Dam, and theKatonga River is choked by papyrus.

In 1991–93 and 1993–94, S. intermedius was found primarily in the peripheralareas of southern and south-eastern Lake Nabugabo (Ogutu-Ohwayo, 1993; Chap-man et al., 1996a). These areas are fringed by extensive marginal wetland and exhibitlow oxygen conditions. Nile perch seem to be less active in the areas close to thewetlands. Both the low oxygen conditions and the structural complexity of the densewetlands may limit exploitation by Nile perch (Chapman et al., 1996a,b), which isintolerant of low oxygen conditions (Fish, 1956; Schofield, 1997).

Since 1995, very few S. intermedius have been caught in Lake Nabugabo, indicatingits continued decline in this lake. The steady decline in the abundance of S. intermediusin Lake Nabugabo, despite reduction in numbers of large Nile perch due to overfishingand the apparent resurgence of some haplochromines, suggests that overfishing may



be another important factor affecting populations of native predatory fishes. BothB. docmac and S. intermedius were coveted species in the neighbourhood of LakeNabugabo. The practice of setting small-sized gill nets in certain areas of the lakehas taken a heavy toll on both juveniles and adults of these species and might havereduced their populations to levels where stochastic events could result in extirpation.

Conclusion

The depletion of the haplochromines in Lakes Victoria, Kyoga, and Nabugabo seemsto have deprived the indigenous piscivores of their preferred prey, leading to decreasedsurvivorship and a dietary shift to alternative prey. The restricted distribution ofsurviving indigenous predators (especially the smaller species and smaller individualsof larger species), and their occurrence in the stomach contents of Nile perch, suggeststhat predation by the latter was another factor that contributed to decline. A fishthat has its foraging success restricted by the presence of predators may experiencereduced growth and reproductive success, and slower growth can also lengthen thetime over which a fish is at risk from a size- or gape-limited predator such as theNile perch. However, the flexibility in diet and habitat exhibited by B. docmac andS. intermedius has permitted populations of these indigenous predators to persist inreduced numbers in Lake Victoria. In the last few years, overfishing of Nile perchhas reduced its population to the point where indigenous predators that have survivedare showing signs of resurgence and may once again diversify the Lake Victoriafishery.

Acknowledgements

Funding for this research was provided by the National Geographic Society, theNational Science Foundation, the Wildlife Conservation Society and a Universityof Florida Grinter Fellowship. We thank J. Mutebi, D. Kasozi, L. Kikwangu, B.Amiina, F. Mugume, B. Ddungu and C. Chapman for assistance with field sampling.Permission to conduct research in Uganda was acquired from the National Ag-ricultural Research Organization, the National Council for Science and Technology,the Office of the President, Makerere University, and the Fisheries Research Instituteof Uganda. We thank F. Nordlie and T. Crisman for comments on an earlier draftof this manuscript.

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(Manuscript accepted 23 February 1999)


Documents

Trophic shifts in predatory catfishes following the introduction of Nile perch into Lake Victoria