Cascading effects of introduced Nile perch (Latesniloticus) on the foraging ecology of Nile tilapia(Oreochromis niloticus)

Introduction

The introduction and successful establishment of non-indigenous fish species in the Lake Victoria Basin ofEast Africa has been followed by dramatic ecologicalchanges. The Nile perch (Lates niloticus L., a largecentropomid piscivore) was introduced into lakesVictoria and Kyoga from lakes Albert and Turkanaduring the 1950s and 1960s to compensate fordepleting commercial fisheries and to improve thegame fishery (Fryer 1960; Ogutu-Ohwayo 1990a,b,1993, 1994; Jackson 2000; Pringle 2005). Althoughmany fish stocks in Lake Victoria had declined prior toexpansion of the Nile perch population, a dramaticincrease in the stock size of Nile perch in the 1980scoincided with a drastic decline in populations ofmany indigenous species, most notably the disappear-

ance of an estimated 40% of the endemic haplochro-mine cichlids (Kaufman 1992; Witte et al. 1992a,b;Seehausen et al. 1997a,b; Balirwa et al. 2003). InLake Nabugabo, a satellite lake of the larger Victoria,Nile perch were introduced in 1960 and 1963, and thepattern of change in fish faunal structure and diversityfollowed that observed in Lake Victoria (Ogutu-Ohwayo 1993; Chapman et al. 1996a,b). Four non-indigenous tilapiines (Tilapia zillii Gervais, Oreochr-omis niloticus, Oreochromis leucostictus Trewavasand Tilapia rendalli Boulenger) were also introducedat various points around Lake Victoria from 1953onwards in response to reduced catch per unit effort(CPUE) of two native tilapiines (Oreochromis escu-lentus Graham and Oreochromis variabilis Boulenger)that were the main target of the local fishermen sincethe beginning of the Lake Victoria fisheries. By 1960,

Ecology of Freshwater Fish 2006: 15: 470–481Printed in Singapore Æ All rights reserved

� 2006 The AuthorsJournal compilation � 2006 Blackwell Munksgaard

ECOLOGY OFFRESHWATER FISH

470 doi: 10.1111/j.1600-0633.2006.00185.x

Bwanika GN, Chapman LJ, Kizito Y, Balirwa J. Cascading effects ofintroduced Nile perch (Lates niloticus) on the foraging ecology of Niletilapia (Oreochromis niloticus).Ecology of Freshwater Fish 2006: 15: 470–481. � 2006 The Authors.Journal compilation � 2006 Blackwell Munksgaard

Abstract – Nile tilapia (Oreochromis niloticus L.) is the dominant of theintroduced tilapiines in many East African lakes and has flourished in thepresence of introduced Nile perch (Lates niloticus L.). We explored thehypothesis that O. niloticus exhibits increased omnivory in response to adecline in abundance of haplochromine cichlids. First, we quantifiedvariation in habitat use and diet of O. niloticus in Lake Nabugabo, Uganda.Second, we compared the diet of O. niloticus in lakes with (Nabugabo,Victoria) and without (Mburo, Wamala, Nyamusingiri, Kyasanduka)introduced Nile perch. In Lake Nabugabo, a higher level ofphytoplanktivory was observed in small juveniles than in larger fish and inwetland ecotone areas where haplochromines were most abundant. Anomnivorous diet dominated by detritus and invertebrates was recorded forO. niloticus in lakes Nabugabo and Victoria, while a predominantlyherbivorous diet was characteristic of O. niloticus in lakes without Nileperch. Availability of a broad food base in lakes where inshore insectivoreshave been reduced may explain the increased omnivory recorded in lakesNabugabo and Victoria.

G. N. Bwanika1, L. J. Chapman2,3,Y. Kizito1, J. Balirwa4

1Department of Zoology, Makerere University,Kampala, Uganda, 2Department of Biology, McGillUniversity, Montreal, QC, Canada, 3WildlifeConservation Society, Bronx, NY, USA, 4FisheriesResources Research Institute, Jinja, Uganda

Key words: non-indigenous species; LakeVictoria; East Africa; diet; habitat use; herbivory

L. J. Chapman, Department of Biology, McGillUniversity, 1205 Avenue Docteur Penfield,Montreal, QC, Canada H3A 1B1;e-mail: lauren.chapman@mcgill.ca

Accepted for publication April 13, 2006

they had also been introduced in lakes Kyoga,Nabugabo, and later into other lakes within the region(Beauchamp 1958; Welcomme 1967, 1988). Of all thenative and introduced tilapiines in the Lake Victoriaregion, it is only O. niloticus, the Nile tilapia, that hasbecome very abundant and commercially important inthe presence of the introduced Nile perch. Thisspecies now forms a critical component of thefisheries of lakes Victoria, Kyoga and Nabugabo,and is of great commercial value in many other smalllakes and dams where it has been introduced. Thefisheries of lakes Victoria and other lakes into whichboth O. niloticus and Nile perch have been introduced(e.g., Nabugabo, Kyoga) now depends primarily onthree species (Nile perch, Rastrineobola argenteaPellegrin, O. niloticus).The successful establishment of non-indigenous

fishes, in particular the O. niloticus and Nile perchin the Lake Victoria Basin, has been attributed toseveral factors including their ability to respondeffectively to a different and dynamic prey base. Thefeeding habits of Nile perch are flexible, such thatwhen preferred items are depleted, the fish shifts toother available prey (Hughes 1986; Ogari & Dadzie1988; Ogutu-Ohwayo 1990b; Chapman et al. 2003).Likewise, the success of some tilapias in colonising awide range of novel habitats has been attributed, ingeneral, to opportunistic food habits, such that food israrely a limiting factor, and their flexibility in growthrate and maturation size according to prevailingenvironmental conditions (Lowe-McConnell 1958;Balirwa 1998; Leveque 2002).Studies on the diet of O. niloticus in both its

indigenous and new habitats in East Africa date backto the early 1950s. Earlier studies described the diet ofO. niloticus as predominantly herbivorous, comprisedmainly of algae, epiphytic diatoms and bottom debris(Fish 1955; Lowe-McConnell 1958; Moriarity &Moriarity 1973). Studies undertaken shortly after theestablishment of O. niloticus in the Victoria regionstill recorded a predominantly herbivorous diet(Welcomme 1967). Recent studies, however, indicatea shift in the dietary composition of O. niloticus toinclude a broad spectrum of items (omnivorous) withhigh proportions of macroinvertebrates and detritus(Gophen et al. 1993; Balirwa 1998). The haplochro-mines of Lake Victoria consisted of several trophicgroups including detritivores, zooplanktivores andinsectivores (Goldschmidt et al. 1993); and theirdisappearance from various waterbodies where Nileperch have been introduced may have resulted invacant trophic niches, leading to an increase ofmacroinvertebrates, zooplankton and phytoplankton(their former main food sources). This would lead toincreased access to a wide food base, which couldpotentially be exploited by O. niloticus.

The overall goal of this study was to explore thehypothesis that O. niloticus exhibits increased omn-ivory in response to a decline in the abundance ofhaplochromine benthivores. We approached this intwo ways. First, we quantified variation in the habitatuse and diet of O. niloticus in Lake Nabugabo,Uganda relative to intralake variation in the abundanceof haplochromines. Second, we compared the dietof O. niloticus in lakes with introduced Nile perch(Nabugabo and Victoria), and lakes without Nile perch(Wamala, Mburo, Nyamusingiri and Kyasanduka).

Materials and methods

Habitat utilisation and diet of O. niloticus in LakeNabugabo

Lake Nabugabo, a satellite of Lake Victoria (24 km2,approximately 0�45¢S, 31�45¢E, see Fig. 1 in Randle& Chapman 2004), is characterised by an extensivestretch of shoreline macrophytes (mainly Miscanthi-dium violaceum and Vossia cuspidata), interrupted bystretches of forests (dominated by Ficus spp.) and sandbeaches. Lake Nabugabo is believed to have beenformed when a sand bar separated a portion of LakeVictoria about 4000 years ago (Worthington 1932;Trewavas 1933; Greenwood 1965, 1966). This satel-lite lake now drains southeastward via the LwamundaSwamp after which the water seeps through the sandbar into Lake Victoria.

To quantify habitat use by different fish species inLake Nabugabo and assess whether food habits ofO. niloticus differ among habitat types, 15 transects(each 550 m in length) were selected to include majorhabitat types within the lake. This included five forestedge transects, five wetland ecotone transects and fiveopen-water transects (350–500 m off the shoreline).Two of the wetland ecotone transects encompassedfloating leafed macrophytes (Nymphea lotus andNymphea caerullea) extending 10–20 m off theshoreline.

Fish specimens, macroinvertebrate samples and asuite of physicochemical characters were collectedonce every 2 months in Lake Nabugabo over a periodof 18 months (February 2000 to August 2001). Fishspecimens were caught using a 550-m long gillnet fleetof various mesh sizes (1–5 in., in increments of 1/2 in.)set for 24 h in each transect; and captured fish werecollected both in the morning and evening (12-hintervals). Gillnets were set as close as possible to theshoreline for the forest edges and wetland habitats. Inaddition, 10 metal minnow traps were set at 50-mintervals along the shoreline for each transect. Spec-imens collected from minnow traps and additionalspecimens from commercial catch were used tosupplement numbers for stomach content analysis.

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471

Each captured fish was identified, and all O. niloticusspecimens were measured for both length (total lengthand standard length, 0.1 cm) and body mass (0.1 g).The stomachs of O. niloticus were dissected out, andstomach fullness was visually assessed at four levels,slightly modified from Ball (1961), where: level 1,empty stomach (0%); level 2, food occupying 1/4 in.of the total volume of the stomach (25%); level 3, foodoccupying 3/4 of the stomach volume (75%); and level4, a full stomach (100%). Stomachs containing foodwere preserved in 10% formalin for subsequentanalysis of dietary content.

During each sampling period benthic macrofaunawere collected at sites using an Ekman grab (with anopening of 225 cm2 and depth of 17 cm) with onegrab per transect. Samples collected were washedseveral times using a macrofauna sieve (250 lm) andpreserved in 5% formalin for subsequent analysis.Macroinvertebrate samples were identified under abinocular microscope and total number of each majortaxa quantified. Physicochemical conditions [Secchidepth (m), dissolved oxygen (mgÆl)1) and watertemperature (�C)] were taken at sites of fish sampling.Dissolved oxygen and water temperature were meas-ured in triplicate just below surface water using a YSIoxygen meter (model 51 B; YSI EnvironmentalIncorporated, Yellow Springs, OH, USA). Secchidepth was measured using a Secchi disc (20 cm indiameter) following standard procedures.

In the laboratory, the mass of stomach contentswas determined, and stomach contents were thendiluted with water for easy visibility under a binocu-lar and compound microscope. Two approaches weretaken during stomach content analyses. First, thecontents were viewed under a binocular microscope,identified and grouped into major dietary items andpercentage contribution of each category establishedby eye using the subjective percentage volumeassessment method outlined by Hyslop (1980).Second, a finer categorisation of the broad categorieswas carried out on three subsamples viewed under acompound microscope (·400). At this stage, a majorfood category was further split into two or threecategories depending on their relative abundances. Totake into account the differences in stomach fullness,the percentage contribution of a food category wasmultiplied by an equivalent percentage of the stom-ach fullness score.

Interlake variation in the diet of O. niloticus

The diet of O. niloticus was compared between lakeswith Nile perch (Lake Nabugabo and Napoleon Gulfof Lake Victoria) and lakes without Nile perch (lakesWamala, Mburo, Nyamusingiri and Kyasanduka).Point-in-time fish sampling was carried out in lakes

Wamala and Mburo as part of this study. Availabledata on food habits of O. niloticus in lakes Victoria(Balirwa 1998), Nyamusingiri and Kyasanduka(Bwanika et al. 2004) were adapted from the literaturefor comparison.

Napoleon Gulf (approximately 133 km2, 0�22¢–0�30¢N, 33�10¢–33�26¢E) lies to the northern part ofLake Victoria comprising several bays and islands.Most of the historical data that exists on the shallowwaters of Lake Victoria in Uganda has been recorded inthe Napoleon Gulf. Lake Mburo (13 km2, 0�38¢–0�41¢S, 30�55¢–31�57¢E) is situated in Lake MburoNational Park, western Uganda. Three species of tilapia(O. niloticus, O. leucostictus and T. zillii) were intro-duced into this lake, but, unlike lakes Victoria andNabugabo, Nile perch has not been transferred to LakeMburo. Other indigenous fish species including O. es-culentus, O. variabilis and haplochromine cichlids arefound in the lake. Lake Wamala (118 km2, 0�15¢–0�25¢N, 31�45¢–32�0¢E) is located approximately75 km north of Lake Nabugabo and 70 km west ofKampala, Uganda. The lake was stocked in 1956 withO. niloticus, O. leucostictus and T. zillii but not Nileperch; and the lake was opened to commercial fishingin 1960. Several other indigenous fish species, inclu-ding haplochromine cichlids are found in this lake.Lakes Nyamusingiri and Kyasanduka (approximately0�16¢S and 0�18¢S – 30�00¢E and 30�04¢E) are shallowcrater lakes (440 and 150 ha, respectively) located inthe Bunyaruguru cluster of crater lakes in WesternUganda. Part of this cluster lies within MaramagamboForest that acts as a catchment of the Eastern escarp-ment of the Rift Valley (Melack 1978; Kizito et al.1993). Lakes Nyamusingiri and Kyasanduka lie at theborder of this forest and grass savanna covered thehills. It is reported that tilapiines, including O. niloti-cus, were introduced to increase fisheries production ofthese lakes (Welcomme 1988; Ogutu-Ohwayo 1990b;Kizito et al. 1993). Bwanika et al. (2004) describedO. niloticus as comprising 8% of experimental catch inLake Nyamusinigiri and 55% of the catch in LakeKyasanduka. Small haplochromine cichlids dominatedthe remainder of the assemblage in both lakes.

Data analysis

Average monthly rainfall data for the period 1985–1998 (Meteorological Department, Kampala 1999)were used to divide the sampling period into two mainseasons: wet and dry season using the annual rainfallmean as the dividing point. CPUE was taken torepresent total number of fish of a given taxa(experimental gill nets only) captured per transect,since effort was approximately 12 h in all samplingtransects. A wet and dry season CPUE value for eachtransect was derived as the average CPUE of all the

Bwanika et al.

472

dry season months and all the wet season months. Toassess temporal and spatial variation in CPUE ofO. niloticus, haplochromine cichlids and Nile perch,macroinvertebrate abundance and physicochemicalconditions, a repeated measures analysis of variancewas used to test for the effect of habitat, season(dry vs. wet) and the interaction of the two onlog10-transformed mean CPUE, and physicochemicalconditions (dissolved oxygen concentration, watertemperature and Secchi depth). Least-squares meanswere used to test for differences in mean values amonghabitats.To explore in more detail the potential relationships

between the abundance of O. niloticus and both theabundance of haplochromines and other environmen-tal variables, we exploited variation among transectswithin Lake Nabugabo. Pearson correlation was usedto test for a relationship between the CPUE ofO. niloticus and the CPUE of haplochromines amongtransects. Both variables were log10 transformed.Stepwise linear regression was then used to detectsignificant environmental predictors of O. niloticusabundance among transects with log-transformedCPUE of O. niloticus as the dependent variable andthe following suite of independent variables: log-transformed macroinvertebrate abundance, dissolvedoxygen concentration, water temperature and watertransparency. Mean dry and wet season values forindividual transects were used in the analyses.

Results

Habitat utilisation and environmental conditions

Season (dry and wet) and the interaction betweenseason and habitat type did not have a significanteffect on CPUE of O. niloticus, haplochromine cich-lids and Nile perch. However, for all the taxa, CPUE

differed among habitats (Table 1). Oreochromisniloticus were more abundant in the forest and wetlandecotone habitat than in the open-water habitat(P < 0.001, Fig. 1). However, no difference wasdetected in the CPUE of O. niloticus between forestand wetland habitat (P ¼ 0.739, Table 1).

Average size of O. niloticus differed among habitatstypes of Lake Nabugabo (anova: F ¼ 11.31,P < 0.001). Oreochromis niloticus were smallest inthe wetland ecotones (mean total length ¼ 17.1 ± 0.5,SE, anova: F ¼ 11.30, P < 0.001), larger in theforest edges (mean total length ¼ 19.7 ± 0.5, SE) andlargest in the open waters (mean totallength ¼ 26.0 ± 5.0, SE, Scheffe post hoc tests,P < 0.05). Haplochromine cichlids were most abun-dant in the wetland ecotone (P < 0.001, Fig. 1). Therewas an overall habitat effect on the abundance of Nileperch; Nile perch were more abundant in inshore areas(forest and wetland ecotone) than in the open water(P ¼ 0.017, Fig. 1).

To explore the relationship between the abundanceof O. niloticus and the abundance of haplochromines,we looked at the correlation between CPUE of the twotaxa across transects. The CPUE of O. niloticus acrosstransects was positively correlated with the CPUE ofhaplochromine cichlids in both the dry season(r ¼ 0.701, P ¼ 0.004) and wet season (r ¼ 0.794,P < 0.001).

We detected no significant effects of habitat, seasonor their interaction on dissolved oxygen concentration(Table 2). Water transparency was higher in the dryseason than in the wet season (P ¼ 0.001), andmarginally higher in the open waters (P ¼ 0.051,Table 2, Fig. 2). Water temperature was lower in thewetland habitats than in the forest edge areas and theopen water (P ¼ 0.009); and temperature was mar-ginally higher in the wet season than in the dry season(P ¼ 0.067, Table 2, Fig. 2).

Table 1. Results of repeated measures analysis ofvariance testing the effects of season (dry vs.wet), habitat and their interaction on log10 catchper unit effort of Oreochromis niloticus, haplo-chromines, and Lates niloticus.

Species Source of variation d.f. Mean square F P

O. niloticus Between subject effects (habitat) 2 3.592 15.550 <0.001Error 12 0.231Within subject effects (season) 1 0.068 0.001 0.972Error (season) 12 0.052Habitat · season 2 0.068 1.312 0.305

Haplochromines Between subject effects (habitat) 2 12.384 48.160 <0.001Error 12 0.257Within subject effects (season) 1 0.117 0.570 0.465Error (season) 12 0.205Habitat · season 2 0.218 1.062 0.375

L. niloticus Between subject effects (habitat) 2 0.858 5.820 0.017Error 12 0.147Within subject effects (season) 1 0.022 0.467 0.507Error (season) 12 0.047Habitat · season 2 0.094 1.997 0.178

Data were collected from five transects in each of three habitat types (wetland, forest, open water) in LakeNabugabo, Uganda.

Foraging ecology of Nile tilapia

473

With respect to macroinvertebrate abundance, boththe habitat and the habitat by season interaction weresignificant indicating that habitat differences differed

between seasons (Table 2). During the dry season,macroinvertebrates were more abundant in the forestedge and open-water habitats than in wetland ecotoneareas (P < 0.001). During the wet season, macro-invertebrates were most abundant in the forest habitat(P ¼ 0.001).

Stepwise multiple regression indicated water trans-parency (Secchi depth) as the only significant predic-tor of O. niloticus CPUE among transects. During thedry season, water transparency explained 46% of thevariation in the CPUE of O. niloticus among transects(F ¼ 11.158, P ¼ 0.005); during the wet season,water transparency explained 33% of the variance inO. niloticus CPUE among transects (F ¼ 6.274,P ¼ 0.026). In both seasons, O. niloticus abundancewas higher where water transparency was lower.

Food and feeding habits of O. niloticus in different habitattypes of Lake Nabugabo

The diet of O. niloticus differed among habitat typesin Lake Nabugabo (Fig. 3a). A greater richness offood categories was recorded in the forest edge andwetland ecotone habitats than in the open-waterhabitat. Fish captured from the open-water habitathad the highest percentage composition of detritus(particulate organic) in their diet. Insects were mainlyconsumed by fish in the forest edge habitat, followedby those in the wetland ecotone habitat. Plantmaterial (which included primarily parts of decom-posing plants) was most frequently consumed in theforest edge habitat, a lower percentage was recordedfor the wetland ecotone habitat, and it was notrepresented in the diet of fish from open waters.Oligochaetes contributed more to the diet of fish in

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Fig. 1. Variation in the mean catch per unit effort (±SE) of fish taxa(Oreochromis niloticus, haplochromines, and Lates niloticus)across three habitat types in Lake Nabugabo, Uganda. Bars thatshare the same letter are not significantly different (least-squaresmeans).

Table 2. Results of repeated measures analysis ofvariance testing the effects of season (dry vs.wet), habitat and their interaction on dissolvedoxygen (mgÆl)1), Secchi depth (m), water tem-perature (�C) and the catch per unit effort (CPUE)of aquatic macroinvertebrates.

Environmental variable Source of variation d.f. Mean square F P

Dissolved oxygen (mgÆl)1) Between subject effects (habitat) 2 0.129 0.202 0.820Error 12 0.640Within subject effects (season) 1 0.016 0.065 0.803Error (season) 12 0.250Habitat · season 2 0.082 0.329 0.726

Secchi depth (m) Between subject effects (habitat) 2 0.017 3.852 0.051Error 12 0.045Within subject effects (season) 1 0.027 18.00 0.001Error (season) 12 0.003Habitat · season 2 0.000 0.000 1.000

Temperature (�C) Between subject effects (habitat) 2 2.324 7.207 0.009Error 12 0.322Within subject effects (season) 1 1.008 4.058 0.067Error (season) 12 0.248Habitat · season 2 0.032 0.130 0.879

Macroinvertebrates (CPUE) Between subject effects (habitat) 2 4.199 17.840 <0.001Error 12 0.231Within subject effects (season) 1 0.841 3.294 0.095Error (season) 12 0.255Habitat · season 2 1.687 6.603 0.012

Data were collected from five transects in each of three habitat types (wetland, forest, open) in LakeNabugabo, Uganda.

Bwanika et al.

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the wetland ecotone than the forest edge or openwaters. Phytoplankton comprised a higher percentageof the diet of fish in the wetland ecotone than theother habitats.

An ontogenetic dietary shift was notable in theO. niloticus of Lake Nabugabo (Fig. 3b). JuvenileO. niloticus consumed a higher percentage of phyto-plankton than large O. niloticus and a lower percent-age of insects and (decomposing) plant materials. Weexplored seasonal variation in diet by calculating thepercentage composition of major prey types for eachsize class in the wet and dry seasons. The smallest size(<10 cm) was not well represented in the dry season;however, in the larger size classes variation in dietcomposition between the dry and wet periods was verymodest. The average per cent difference between dryand wet season values across prey types was only2.1% with a range of 0–9.7%.

Dietary composition of O. niloticus among lakes

Across habitats and size classes, the diet of O. niloti-cus in Lake Nabugabo included at least five majorfood categories: detritus (most dominant), followed byinsects, plant material, oligochaetes and phytoplankton(Fig. 4). Chironomid and ephemeropteran larvae werethe major insects consumed. Phytoplankton compriseda relatively small component of the diet, and consistedof blue green algae (Microcystis and Anabaena; mostdominant), followed by diatoms and green algae(Scenedesmus). A similar trend was recorded byBalirwa (1998) for O. niloticus from the inshore areasof Napoleon Gulf, Lake Victoria (Fig. 4). Detritusdominated the composition of the diet in these tilapia(43%) followed by insects (30%, primarily chirono-mids); while phytoplankton was rare (6%, Fig. 4).

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Fig. 2. Variation in mean levels (±SE) of (a) dissolved oxygen(mgÆl)1), (b) Secchi depth (m) and (c) surface water temperature(�C) among three habitats (forest, open water and wetland ecotone)in Lake Nabugabo, Uganda. Bars that share the same letter are notsignificantly different (least-squares means).

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Fig. 3. Percentage composition of foodtypes in the stomachs of Oreochromis nil-oticus in (a) three different habitat types(forest edge, open water and wetland eco-tone) and (b) across four size classes of Niletilapia, Oreochromis niloticus, from LakeNabugabo, Uganda. Sample size is indicatedfor each size group.

Foraging ecology of Nile tilapia

475

The diet of O. niloticus in lakes Wamala and Mburodiffered from that recorded in lakes Nabugabo andVictoria (Fig. 4). Phytoplankton dominated the diet[58% and 43% in lakes Wamala (N ¼ 87 non-emptystomachs) and Mburo (N ¼ 25), respectively], fol-lowed by detritus (34% and 32%, respectively). Themajor phytoplankton taxa recorded were Chlorophyta(dominated by Scenedesmus) and Cyanophyta (dom-inated by Microcystis). Minor consumption of insectswas recorded in lakes Mburo (4%) and Wamala(about 2%). Similarly, in lakes Nyamusingiri andKyasanduka, O. niloticus consumed mostly phyto-plankton (Fig. 4). Chlorophyta (mainly Scenedesmus)were more abundant than Cyanophyta (mainly Micro-cystis) in the diet of O. niloticus in Lake Nyamusing-iri, while the phytoplankton consumed by fish in LakeKyasanduka was completely comprised of Cyan-ophyta (mainly Microcystis). Noticeably, neither det-ritus nor aquatic insects constituted a significantproportion of the diet of O. niloticus in lakesNyamusingiri and Kyasanduka.

Discussion

Habitat use and diet of O. niloticus in Lake Nabugabo

Within Lake Nabugabo, Oreochromis niloticus wasmore abundant in inshore areas (forest edge andwetland ecotone) than in the open waters, as were Nile

perch; haplochromine cichlids were most abundant inwetland ecotone habitats. Over the range of transectswithin the lake, the abundance of O. niloticus waspositively correlated with the abundance of haplo-chromines. Of the environmental variables considered(macroinvertebrate abundance, water transparency,dissolved oxygen and water temperature), watertransparency was the only significant predictor ofO. niloticus CPUE.

Although the productivity (both primary and sec-ondary) of inshore habitats has been strongly correla-ted to fish abundance (Macdonald 1956; Rasmussen1988; Okedi 1990), relative availability of food itemsdoes not fully explain the habitat use of O. niloticusobserved in this study. The highest density of macro-invertebrates (a major dietary item) was recorded inthe forest edge and open-water habitats during the dryseason and in the forest edge habitats during the wetseason, but there was no seasonal effect on CPUE ofO. niloticus. In addition, the density of macroinverte-brates was not a significant predictor of CPUE ofO. niloticus among transects. However, preference forhabitat conditions less favourable to the huntingefficiency of Nile perch may, to some extent, explainthis pattern of habitat use. The use of highly structuredor shallow inshore areas where predation risk isreduced is common among juvenile fishes (Mittelbach1981; Werner et al. 1983; He & Kitchell 1990; Brown& Moyle 1991). Despite the relatively high CPUE of

Detritus34%

Plant material4%

Others4%

Cyanophyta32%

Other algae7%

Phytoplankton58%

Chlorophyta19%

Phytoplankton43%

Detritus32%

Plant material21%

Insects4%

Zooplankton7%

Others5% Chlorophyta

75%

Cyanophyta13%

Phytoplankton88%

Insects2% Zooplankton

8%

Others11%

Phytoplankton79%

Lake Wamala

Lake Mburo

Lake Nyamusingiri

Lake Kyasanduka

Detritus54%

Plant material12%

Oligochaetes7% Phytoplankton

6% Others 1%Ephemeroptera

3%Chironomids

17%

Insects21%

Detritus43%

6%

6%Others

10% Molluscs5%

Chironomids22%

Caridina 4%Others 4%

Insects30%

Plant material

Phytoplankton

Lake Nabugabo Lake Victoria

Fig. 4. Percentage composition of the foodcategories in the diet of Nile tilapia Ore-ochromis niloticus, in four Ugandan lakeswith introduced Nile perch [Lake Nabugabo(current study) and Lake Victoria (adaptedfrom Balirwa 1998)] and lakes without int-roduced Nile perch [Lake Wamala and LakeMburo (current study) and Lake Nyamus-ingiri and Lake Kyasanduka (adapted fromBwanika et al. 2004)].

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Nile perch that we observed in inshore areas in thisstudy, there is good evidence to indicate that thestructurally complex wetlands of Lake Nabugaboprovide refuges for several indigenous fish species,and the introduced O. niloticus, from predatory Nileperch (Chapman et al. 1996a,b; Rosenberger &Chapman 1999; Schofield & Chapman 1999). Theprevalence of O. niloticus in habitats with low watertransparency may reflect a relationship between tilapiaand another variable that is correlated to watertransparency. However, it is also possible that thelower transparency provides some additional protec-tion from Nile perch.In general, results from the different habitats of

Lake Nabugabo indicate that O. niloticus has a varieddiet consisting of five (offshore habitat) to eight(inshore habitat) major dietary categories. Theseobservations agree with other recent findings suggest-ing that O. niloticus presently has an omnivorous dietin lakes with introduced Nile perch (Gophen et al.1993; Balirwa 1998). There were, however, distinctdifferences in the percentage contribution of differentfood categories among habitats. The large contributionof detritus and complete lack of plant material in thediet of O. niloticus from open-water habitats suggestsfood availability as a plausible source of the habitateffect, as plant parts are more rare in these open-waterareas than the inshore habitats. Similarly, the relativelygreater contribution of insect larvae to the diet ofO. niloticus from the forest edge habitat may reflectthe high abundance of insect larvae recorded from thishabitat. The highest consumption of phytoplanktonoccurred in the wetland ecotone habitat, while insectfeeding was lower than in the inshore forested areas.As haplochromines were most abundant in the wetlandecotones and as the CPUE of O. niloticus waspositively correlated with haplochromine abundance,the diet characteristics of O. niloticus may reflectincreased competition for invertebrates in this area.Three of the six haplochromine species whose diet wasinvestigated by Greenwood (1965) in Lake Nabugabopredominantly fed on macroinvertebrates. Higherlevels of phytoplankton consumption in wetlandecotones also relates to the interaction of size and dietin O. niloticus of Lake Nabugabo. Juvenile O. niloti-cus tend to occupy nearshore sheltered habitats (e.g.,wetland ecotones, Moriarity et al. 1973; Balirwa 1998;Gooudswaard et al. 2002; this study), and in LakeNabugabo, juvenile O. niloticus exhibited a higherlevel of phytoplanktivory than the larger size classes.This is a particularly interesting finding that is notconsistent with the study of O. niloticus in LakeGeorge, Uganda. In Lake George, Moriarity et al.(1973) found that young O. niloticus below 6 cm intotal length engaged in active pursuit and ‘pecking’ toinclude a variety of animal and plant materials in their

diet (omnivorous), while larger fish were mainly filterfeeders characterised by a primarily phytoplanktivor-ous diet. It is possible that juvenile O. niloticus selectstructured inshore areas, and in doing so are using ahabitat that exposes them to higher levels of compe-tition, and therefore influences their diet.

Cascading effects of the predatory Nile perch andprobable vacant trophic niches

Comparisons of the diet of O. niloticus among lakesindicate an omnivorous diet dominated by detritus andinvertebrates in lakes Nabugabo and Victoria and apredominantly herbivorous diet in lakes Wamala,Mburo, Nyamusingiri and Kyasanduka. We believethat this may reflect the introduction of Nile perch intolakes Nabugabo and Victoria and the cascading effectson the food web. Oreochromis niloticus has beendescribed as an herbivore in numerous earlier studies(Fish 1955; Lowe-McConnell 1958; Moriarity 1973;Harbott 1975; Getachew 1987). Moriarity (1973),using 14C-labelled monospecific cultures of algae fedto fish, found that O. niloticus assimilated a maximumof 70–80% of ingested carbon from the blue-greenalgaeMicrocystis sp. and Anabaena sp. and the diatomNitzschia, while a maximum of 50% was assimilatedfrom green algae Chlorella sp. Consequently, thedominance of tilapiine fishes in tropical lakes has beenattributed to their efficient utilisation of blue-greenalgae or detritus (Getachew 1987). Following theintroduction of O. niloticus to Lake Victoria their dietconsisted of planktonic and bottom materials as themajor dietary items (Welcomme 1967; Harbott 1975).Oreochromis niloticus now exhibits a more diversediet in Lake Victoria (Balirwa 1992, 1998; Gophenet al. 1993; Getabu 1994) and a similarly omivorousdiet in Lake Nabugabo. The observed omnivorous dietof O. niloticus in lakes where inshore insectivoreshave been reduced by the predatory Nile perchsuggests availability of a broader food base than waspotentially available when other competitors existed(Balirwa 1998).

Loss of fish species in lakes of the Victoria Basinhas contributed, at least in part, to a massive change introphic structure (Balirwa et al. 2003). Among thehaplochromines that either disappeared or were greatlyreduced from Lake Victoria, the detritivore–insecti-vores were the most abundant group constituting54.5% of the haplochromine biomass followed byzooplanktivores at 27% and insectivores at 9.7%(Goldschmidt et al. 1993). In the Mwanza Gulf ofLake Victoria, bottom-dwelling detritivores and thepelagic phytoplanktivores declined by a factor of athousand or more coincident with the Nile perchexplosion (Witte et al. 1992a,b). In the early 1990s,30 years subsequent to the establishment of the Nile

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perch in Lake Nabugabo, a drastic loss of fish specieswas also recorded (Ogutu-Ohwayo 1993). Of the eighthaplochromine cichlids recorded from Lake Nabugabobefore the upsurge of Nile perch (CNBS 1962), onehad vanished; others were very scarce at this time andwere mainly encountered in marginal macrophytes(Ogutu-Ohwayo 1993). Although the fisheries of theLake Victoria Basin had declined before the Nile perchwas introduced, mainly a result of overfishing and ashift to small mesh-sized gill nets, it is generallybelieved that Nile perch contributed to the dramaticdecline observed following its establishment in lakesVictoria, Nabugabo and Kyoga (Ogutu-Ohwayo1990a,b, 1993; Witte et al. 1992a,b; Chapman et al.1996a,b; Balirwa et al. 2003). The disruption andreduction of the diverse and trophically complexindigenous fish community, and most especially thatof the haplochromine cichlids, seems to have initiatedchanges in food web structure. In Lake Victoria, therecent increase in algal production, decrease in watertransparency (Mugidde 1992, 1993) and apparentincrease in the abundance of lake flies (Kaufman1992) are some indicators of an altered lake trophicstructure. The disappearance of haplochromines maywell have allowed the increase of their former mainfood sources including macroinvertebrates, zooplank-ton and phytoplankton.

Oreochromis niloticus, a generalist feeder, seems tohave exploited the wider food base and potentiallyfood items that offer a higher caloric content. Inter-estingly, blue-green algae (Microcystis sp. and Anab-aena sp.), the green algae (Chlorella sp.) and thediatom Nitzschia, well assimilated by O. niloticus(Moriarity 1973) commonly occur in the lakes understudy (Bwanika et al. 2004; Mugidde 1993), suggest-ing that O. niloticus has the opportunity to feed onphytoplankton, but selects a broader diet. Whether anomnivorous diet promotes better growth characteris-tics compared to a phytoplanktivorous diet requires abetter understanding of the bioenergetics of O. niloti-cus and growth/diet studies across a broader range oflakes. However, it should be noted that the growth rateof O. niloticus in Lake Nabugabo is significantlygreater than in conspecifics from Lake Wamala wherethey feed primarily on phytoplankton (Bwanika 2005)suggesting an energetic advantage to the omnivorousdiet.

A growth advantage afforded by an omnivorous dietmay have contributed to the success of O. niloticus inLake Victoria over other tilapiines that do not exhibitsuch dietary flexibility (e.g., O. leucostictus which isprimarily a phytoplanktivore, Balirwa 1998). A widerhabitat tolerance for spawning and nursery groundsthan other tilapiines (Twongo 1995) and assumedaggressiveness towards other species on breedinggrounds (Lowe-McConnell 2000) may also have

facilitated the success of O. niloticus in lakes withintroduced Nile perch.

Similar changes in diet as described for O. niloticushave also been observed for the cyprinid Rastrineo-bola argentea in Lake Victoria. In contrast to manyhaplochromine cichlids in Lake Victoria, the zoo-planktivorous cyprinid R. argentea strongly increasedin numbers, despite serving as prey for Nile perch(Wanink 1998, 1999; Wanink & Witte 2000). Theincrease has been attributed to a relaxation ofcompetitive pressure by haplochromine cichlids sub-sequent to the Nile perch upsurge (Wanink & Witte2000), during which time R. argentea began to exploitthe bottom areas of the lake during the daytime (ahabitat previously occupied by haplochromines) andinclude benthic macroinvertebrates in its diet.

Recently, an increase in the fishing pressure on thelarge-sized Nile perch has coincided with a resurgenceof some haplochromine cichlids in lakes Victoria,Kyoga and Nabugabo (Seehausen et al. 1997b; Witteet al. 2000; Balirwa et al. 2003; Chapman et al. 2003).This study in Lake Nabugabo was conducted at a timewhen haplochromine cichlids had already begun toresurge (Chapman et al. 2003). Oreochromis niloticusmay have exhibited a higher degree of omnivory in theearly 1990s when haplochromine cichlids had beengreatly reduced and will most likely shift to a morerestricted diet if haplochromine cichlids re-establish athigh density.

Interestingly, the resurgence of the zooplanktivor-ous cichlid Haplochromis pyrrhocephalus in LakeVictoria provides additional evidence for cascadingeffects of the Nile perch introduction. This cichlid hadalmost completely disappeared from Lake Victoriaafter the Nile perch upsurge. The species reappeared inthe late 1990s (Katunzi et al. 2003), but with a dietthat included a higher percentage of insects, shrimp,fish and mollusks. Katunzi et al. (2003) argue that anincrease in profitable prey and a decline in theabundance of efficient competitors may have contri-buted, at least in part, to the dietary shift in thisspecies.

Management of the current fisheries of the Victoriaregion, and the aquatic systems that support them willrequire a greater knowledge of food web ecology.Recent changes in the trophic structure of LakeVictoria relate, in part, to fish species introductionsand cascading effects on the ecosystem. In general,much attention has been paid to Nile perch in LakeVictoria over the past three decades, but relatively lessattention on the developments of O. niloticus and inparticular the implications of its feeding habits. This isdespite the fact that success of this species in lakeswhere it has been introduced has been attributed toits flexible feeding habits. Oreochromis niloticuscurrently contributes significantly to commercial

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fisheries, only second in importance to Nile perch.Understanding the recent developments in the feedinghabits of O. niloticus is critical to predicting its futuresuccess in a seemingly dynamic lake environment. Therecently observed resurgence of haplochromine cich-lids and other indigenous fish species may continue toalter the trophic state of these systems. It is probablethat O. niloticus may once again shift to its previouslyherbivorous diet if the observed resurging fish speciesre-establish in their former trophic positions and at highdensity. Such a transition may impact both the growthand condition of Nile tilapia in these systems.

Acknowledgements

Financial support to conduct this study was obtained from theLake Victoria Environment Management Programme (LVEMP)as part of a PhD Scholarship to Gladys N. Bwanika. We wish tothank the Staff of the Department of Zoology, MakerereUniversity and of the Fisheries Resource Research Institute forsupport given during the course of this study.

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