Food habits and trophic resource partitioning among three mormyrid fishes from man-made Lake Ayame, Ivory

Coast
E.P. Kouamelan", T. Kone', V. N'Douba' & F. Ollevier^
Uniuersiti de Cocody Abidjan, UFR Biosdences, Laboratoire d'Hydrobiologie, 22 BP 582 Abidjan 22, Ivory Coast
2

KathoUeke Universiteit Leuven (K.V.L), Zoological Institute. Laboratory of Ecology and Aquaculture, Naamsestraat 59, B-3000 Leuven, Belgium
Received 29 Seplembar 2005 Accepled 18 April 2006

Feeding habits and trophic relationships among three mormyrid species {Petrocephalus bovei, Marcusenius ussheri and Marcusenius furcidens) were assessed in the man-made Lake Ayame in Ivory Coast. The index of preponderance combining the occurrence and weight percentages of the identified prey items showed that these three mormyrid species mainly feed on invertebrates, especially aquatic insects. Petrocephalus bovei mainly feeds on chaoborid larvae, whereas both Marcusenius species preferentially feed on chironomid larvae. This segregation of food items associated with the relative abundance of chironomid larvae may reduce interspecific competition between these three fish species, and may therefore allow their coexistence. Horn's food overlap index revealed highly significant similarities in the trophic spectrum between both Marcusenius species, and for the dry as well as the rainy season. Key words: Mormyridae, feeding, competition, man-made lake, Ivory Coast, West Africa.

INTRODUCTION
in a natural aquatic ecosystem, trophic conditions are one of the most important ecological factors to which fish species must adapt their lifestyles. Several species in the same habitat may use different trophic resources and, in fishes, trophic guilds linked to species behaviour are well known. Trophic resources, habitat diversity and feeding activity rhythms constitute three other major concepts that allow an understanding of the coexistence of species in a given ecosystem (Schoener 1974; Toft 1985; Hori 1987; Leveque 1997), Moreover, species using the same resources have similar ecological requirements {Root 1967; Allan 1995). Consequently, competition among species of the same feeding guild is expected to be high (Greenberg 1991). Trophic resource partitioning may be one of the most important factors by which ecologically similar species coexist. Several works focusing on this field showed a correlation between trophic component diversity and its availability and community structure, and this has been noted in birds (Diamond 1970; Snow & Snow 1972), reptiles (Taylor 1984) and fishes (Zaret & Rand 1971; Angermeier 1982; Martin 1984; Ross 1986; Gibson & Ezzi 1987; Scrimgeour & Winterbourn 1987;
*Author for correspondence. E-mail' kesseich2CX)2@hoImail com

Esteves & Galetti 1995; Esteves 1996; Marshall & Helliott 1997; Hajisamae et al. 2003). Most of thi.' papers published on fishes concern fish data from European and North American temperate areas, and from south American and Asian tropical habitats. In tropical Africa, few papers have focused on the trophic relationships between fish species inhabiting the same habitat (Lauzanne 1983,1988; Ulyel et ai 1990; Goldschmidt et ai 1991). Fish species studied in the present work belong to the family Mormyridae. This freshwater fish family is endemic to Africa and is characterized by the presence of an electric organ located in the caudal peduncle. This organ produces an often species-specific discharge for electro-location and communication (Hopkins 1981). Mormyrid fishes are also considered to be bio-indicator species (Hugueny etal. 1996) as they are among those fishes that react first to environmental change. Previous studies on feeding in the family Mormyridac indicate that most mormyrid species feed on benthic invertebrates (Lauzanne 1988; Kouamelan etal. 1999,2000). This study provides (1) a qualitative and quantitative assessment of the diet of three mormyrid species, (2) examines the variation in diet with season, and (3) assesses the degree of dietary overlap between the three species.

African Zoology 41 (2): 266-274 (October 2006)

Kouamelan et al.: Resource partitioning among mormyrid fishes from Lake Ayame. Ivory Coast

267

GULF OF GUINEA 0

330'

Fig. 1. Map of the Bia River (Ivory Coast) showing the man-made Lake Ayame and the two sampling stations (O).

pled between 0.5 and 1 m deep using an Ekman dredge (15 x 15 cm = 0.225 m"). Ten samples were taken at each of the sites from January to October Sampling area The present study was conducted in the man- 1997. In the laboratory, all benthic organisms in the ninde Lake Ayame built in the Bia River basin in samples were sorted, identified and counted. In W59 in Ivory Coast (Fig. 1). With a surface area of this study data presentation and analysis are 197 km^ and a depth of 30 m, this lake can hold up based on numerical abundance of invertebrates to 1.4 X K)'' m' of water when overflowing (Vanden captured in the benthos samples. Bossche & Bernacsek 1990). This lake is also characterized by a muddy substratum, limited light Stomach contents anal\fsis penetration and a low conductivity (Kouamelan et Two fleets of gill nets, each measuring 30 m long at. 1999). Two sites, Bakro (533'N, 3n5'W) and and 2.5 m deep with mesh sizes of 10,12,15,20,25, Ayame (5''36'N, 3''10'W), were sampled each month 30, 35, 40 and 50 mm were used to collect fish Irom November 1996 to October 1997. This sam- samples. At each sampling site, fishing was done at pling period covered two dry seasons (December night. Gill nets were set at 17:(K) and visited at 1996 - March 1997 and August/September 07:00. 1997) and two rainy seasons (April - July 1997 and A total of 321 mormyrid specimens was examOctober/November 1997). ined:Marcusemusussheri{Cunther,lS67){n = 168), Marcuseiiiiis fiircidens (Pellegrin, 1920) ( = 93) and Invertebrate data Petrocephalus hwei (Valenciennes, 1846) {n = 60). At each of the sampling sites, benthic organisms In the field, all fish specimens captured were (main food items of mormyrid fishes) were sam- identified following Bigorne (1990). Each specimen

MATERIALS & METHODS

268

African Zoology Vol. 41, No. 2, October 2006

was weighed to the nearest 0.1 g, measured to (4) Food overlap (Ci) index of Morisita (1959), as the nearest 1 mm and dissected to remove the modified by Horn (1966), was used to assess stomach, Stomachs were preserved in a 5% the degree of feeding overlap between morformalin solution. myrid species: In the laboratory, the contents of each stomach were removed, mixed with 10 ml water and filtered through 1000, 500 and 100 ^m meshes for easy separation of prey items. Subsequently, the prey taxa were sorted, counted and weighed to the nearest 0.0001 g. All prey items were identified to where s is the total number of food items, and the lowest possible taxon according to Dejoux et al. J, and y, represent the proportion of a type ot (1981) and Died & Ring (1992). prey / eaten by species x and y, respectively. In Four indices for the importance of each prey the present study, food overlap index (CX) was item were calculated. These were: calculated with the (/p) value of each prey. 1) Corrected occurrence percentage (Fd) (Gray The food overlap index {CX) may vary from 0 et ai 1997; Rosecchi & Nouaze 1987): (when samples are completely different) to 1 (when samples are identical). The feeding habits of two species were considered to overlap significantly when a > 0.60 (Zaret & Rand 1971). where f, represents the frequency of prey (', ii, Spearman's correlation coefficient was used to the number of stomachs containing prey i and compare different food habits. Nj the total number of full stomachs examined; 2) Weight percentage (W) (Hyslop 1980): RESULTS Benthic invertebrate data Benthic organisms sampled during the present study were numerically dominated by molluscs and chironomid and chaoborid larvae (Fig. 2a), However, their numerical abundance varied between seasons. High relative abundance of molluscs was observed during the dry season (lanuary-March and August/September) with two maxima (February and September). Molluscs were numerically less abundant during the rainy season (April-July). Analysis of insect data (the main food resource of mormyrids) from the benthos sampies (Fig. 2b) showed that chironomid larvae were numerically more abundant at the beginning of the rainy season (April/May), with a maximum in May, and at the beginning of the dry season, with a maximum in August. The numerical abundance of chaoborid larvae was higher in March (end of the dry season) and in June (rainy season). The other insects (other Diptera, Ephemeroptera, Coleoptera, Odonata and Trichoptera) were only weakly represented. Diet data
Food composition

where w- represents the total weight of prey i and Wj the total weight of all prey; 3) The index of preponderance (Ip) (Natarajan & Jhingran 1961), combining the occurrence and weight percentages, was used to assess the relative importance of each type of prey:

The index of preponderance (1^,) varies from 0 to 100. Different prey taxa were arranged according to the classification scale of Simenstad (1979), used amongst others by Rosecchi & Nouaze (1987): first, the index value of each prey is expressed as a percentage of the total index (2/P); the items are then arranged by decreasing index value; to the item with the highest index value, the index value of each of the prey is added so as to obtain 50% or more of the total index; these prey are considered to be preferential ones. Those prey for which the index value added to that of the preferential, reachies at least 75%, are considered as secondary prey. All the other categories of prey from the list represent incidental prey. Using this classification, if a prey item reached 50% or more, it was considered as preferential.

The qualitative analysis of all stomach contents revealed 15 prey taxa, arranged into four groups

Kouam6lan et al/. Resource partitioning among mormyrid fishes from Lake Ayame, Ivory Coast
5000 4500

269

(a)
-o Chironomidae - Chaoboridae - * ~ Other Insects

:,

3500
3000

-X-Molluscs

> S
2000 1500 1000 500
I!

Jt

Months

1600-1 1400 ^
a

(b) Chironomidae Chaoboridae Other Insects

1200

~ 1000

s
I
b

800
600

B I

400
200

M J Months Fig. 2. Numerical abundance of invertebrates (individuals/m^) sampled between 0.5 and 1 m depth in Lake Ayame (Ivory Coast) from January 1997 to October 1997; a, all benlhic organisms; b, insects in the benthos samples.

(Table 1): insects (10 prey taxa), crustaceans (three prey taxa), molluscs and arachnids (one prey laxon each). No sand was found in the stomach contents of Petrocephalus bovet. Moreover, an important sedimentary fraction composed of sand and mud was noted in al! stomach contents of
Marcusenius furcidens and M. ussheri. Although

sand may be very important in abrading exoskelfton, this fraction has no nutritional value. It was therefore excluded from all the quantitative

values. The index of preponderance indicated that Petroccphahis bovei fed mainly on chaoborid larvae {Ip = 85.54%) and used chironomid larvae (/,. = 12.87%) as additional food items. Insects, particularly chironomid larvae, constituted the main food resource of M. furcidens (/p = 74.42%) and M. ussheri (i,, = 83.38%). These species used Ephemeroptera as secondary prey. Molluscs, arachnids and crustaceans were incidentally ingested by these Marcusenius species.

270

African Zoology Vol. 41, No. 2, October 2006

Table 1. Relative importance expressed by the index of preponderance and classification of prey organisms identified in the stomach contents of three mormyrid species from Lake Ayame, Ivory Coast. Prey taxa Petrocephalus bovei n = 60 Marcusenius ussheri n=168 Marcusenius furcidens

n-93

INSECTS Diptera Chironomidae Aedes sp. Ceratopogon sp. Chaoboridae Tipula sp. Odonata Phyllomacromia sp. Cerbagrion sp. Ephemeroptera Povilla sp. Caenodes sp. Trichoptera Ecr)omus sp. MOLLUSCS Biompharia sp. CRUSTACEA Ostracoda Cladocera Chydorus sp. Diaphanosoma excisum ARACHNIDA Hydracarina sp.

12.87 + 0 0.04 + 85.54 +++ 0 0 0 0.12 + 1.31 + 0.09 +

83.38 0.03 0.02 1.4 0 0.1 0.01 2.23 11.98 0.43

+++ + + +

74.42
0

+++

0.003 + 1.64 +
0.0001 +

+ + + + +

0.64 + 0.005 + 1.04 21.67 0.58 + ++ +

0 0
0 0 0

0.004 + 0.000 + 0.000 + 0.000 + 0.004 +

0.003 + 0.002 + 0 0.001 + 0.01 +

+++ = preferential prey; ++ = secondary prey; + = incidental prey; n = number of specimens examined.

preponderance (/p) indicated feeding similarity Seasonal variations in the composition of the between species belonging to the same guild. diet of mormyrid species were noted in the present Overlap values between Mareusenius species and study (Table 2). In P. hovd, the variation in the diet P. bovei were low {CX = 0.16), indicating that Ihey in relation to seasons was not significant (P > 0.05). feed on different food items. On the other hand, Chaoborid larvae were the main food item of highly significant overlap values were noted beP. bovei in both seasons. In M. furcidens, chironomidtween M. fureidens and M. ussheri {O. = 0.98). larvae dominated the diet in both the dry season During both seasons, no significant food overlap {Ip = 79.92) (December-March and Augiist/Sep- was observed between P. bovei and Marcusenius tember) and the rainy season {Ip ^ 72.06) (April- species (Table 3). On the contrary, during both July and October/November). In M. ussheri. the seasons significant food overlap was noted only diet was also dominated by chironomid larvae in between M. furcidens and M. ussheri. both seasons (/p respectively 85.24 and 64.52). However, during the rainy season, the importance DISCUSSION of this main prey decreased whereas the number Several methods have been used to study stomach of additional prey items (Ephemeroptera larvae) contents in fishes (such as percentage occurrence, increased. This trend was also apparent in M. furci- numerical percentage, percentage weight or voldens. These variations were, however, not signifi- ume). Any of these methods used alone cannot cant (P > 0.05). fuliy reflect the importance of dietary components (Hyslop 1980; Rosecchi & Nouaze 1987). For appropriate characterization of feeding babits of Vood overlap Overlap values {CX) calculated from the index of fishes, mixed indices combining two or three

Seasonal variation in the diet

Kouamelan et ai: Resource partitioning among mormyrid fishes from Lake Ayame, ivory Coast

271

Table 2. Seasonai variation of the reiative importance (/p) of prey organisms identified in stomach contents of three mormyrid species from Lake Ayame. Ivory Coast. Prey taxa Petrocephalus bovei Marcusenius ussheri DS (n=121) 85.24 1.4 1.54 11.13 2 0.06 0.001 0.001 0.001 WS (n-47) 64.52 0.6 0.61 33.67 0.06 1.1 0.02 0.001 0.01 Marcusenius furcidens DS (n = 33) 79.92 0.59 0 17.92

DS
[n = 39) Chironomidae Chaoboridae Other Diptera Ephemeroptera Odonata Trichoptera Molluscs Crustacea Arachnida 17.21 80.01 0.11 2,63 0 0.02

WS
(n = 21) 19.52 78.84 0.01 1.09 0 0.48

WS
(n = 60) 72.06 2.17 0.005 24.36 0.10 0.92 0.001 0.003 0.01

0 0 0

0 0.03 0

1.45 0.11 0.01 0

0.002

DS = dry season (December to March and August/September); WS - rainy season (April to July and October/November); n = number of specirnens examined.

methods hiive been proposed (Windell & Bowen Table 3. Food overlap calculations comparing seasonal differences among mormyrid species from Lake Ayame, 1978). The index of preponderanct- (/p) combin- Ivory Coasl. ing the percentage occurrence and percentage weight, and already used by King et al. (1991) and Dry season Kouamelan et at. (2000) in similar studies, seems M. furcidens M. ussheri P. bovei the most appropriate for studying the feeding c habits of mormyrid species. tn Resulta from benthic invertebrates showed that a M. furcidens 0.21 0.98* (A M. ussheri .imong trophic resources available in the benthos 0.22 0.98' sampled from man-made Lake Ayame, only 0.23 0.25 P bovei chironomid larvae and chaoborid larvae were the (C main food items ofthe mormyrid species. These two Significant food overiap ( Q < 0.6). items were available in the benthos samples throughout the year, with some fluctuations predators. The feeding strategy of the predator between seasons. Angermeier (1982) noted that also plays important role in prey choice (Garcia fluctuations in the availability of food types may et al. 1996). The avoidance of molluscs by moraffect all aspects of animals' foraging and diet to myrid species may be due to their indigestible some extent. In the present work, seasonal fluctua- hard shells, which need specialized anatomic tions of these two main food items seem to have structures such as massive teeth and thick pharynhad no significant influence on the feeding habits geal bone to crush (Kone 2000). These structures of either P. hovei or the Marcusenius species. On theare found in malacophagous fishes (Chimbari et al. uthcr hand, their availability and their relative 1996), but not in mormyrids. abundance, compared to all other trophic food Among the mormyrid species studied, only the items used by mormyrid species, suggest that they food habits of P hovei has been well investigated may play an important role in reducing competi(De Merona 1980; Hyslop 1986). These previous tion between species belonging to the same guild. works done in riverine habitats showed that the Moreover, in spite of their relative numerical species fed mainly on chironomid and Ephemerabundance in the benthos samples, very few optera larvae and on adults of Ht-miptera. Although molluscs were found in the stomach contents the main characteristic of the food habits are of Marcusenius species and none of this trophic similar, being insectivorous, P. bovei in Lake Ayame resource was used by P. bmvi as food items. In a used chaoborid larvae as the main food item. The natural aquatic system, Moore & Moore (1976) ecology of each type of habitat (lake or river) may noted that several factors influenced the choice of account for the observed difference in food comprey items: prey size, availability, distribution, position. Recent work on benthic invertebrates moHlity, vulnerability and its capacity to escape from Bia River by Diomand^ & Gourene (2005)

272

African Zoology Vol. 41, No. 2, October 2006

This paper forms part of the VLIR's (Flemish Interuniversity Council) project 'Evolution of fish diversity after the construction of a man-made There is no published information on the food lake: the caseofthe Bia River', financed by Belgian habits of M, furcidens and M. ussheri. The present Cooperation. We thank J.N. Kouassi for his supstudy provides the first detailed data on the diet of port of the VLIR Project. The authors thank E. these species. Owing to the importance of sand Vreven for his constructive comments on the and mud in the stomach contents examined, we manuscript prior to submission and we thank the suggest that these Marcusenius species are benthic two reviewers for their useful comments that coninsectivores. This benthic behaviour was also tributed to the improvement of the paper. noted by Kouamelan et al. (1999) in Mormyrus
rume.
REFERENCES

only recorded chaoborid larvae in the lacustrine localities. Chaoborids were not sampled in the riverine part of the Bia River. While P. bovei fed on benthic invertebrates, no sand and mud were noted in the stomach contents. Several reasons can account for this species' feeding habits: 1) P. bovei is a pelagic fish (De Merona 1980), 2) all full stomachs of P. bovei were sampled at night, suggesting that the species has a nocturnal feeding habit, and 3) chaoborid larvae that constituted the main food item are known to undertake vertical migrations from the bottom to the surface at night to feed on zooplankton (MacDonald 1956; Witte 1984), suggesting that this prey item is available for P. hovei during its feeding period (at night). While these conclusions should be treated with caution because of the small sample sizes, nocturnal feeding behaviour has also been noted in other mormyrid species by Arrington et ai (2002).

success. Leveque (1997) indicated that when different species' niche overlapped, competition was most likely to occur. On the other hand, Hutchinson (1965) showed that when populations of two species shared the same resources, one of them disappeared in the long term. In the present work, the main feeding component (chironomid larvae) shared by both Marcusenius species may not be in short supply as this prey item constituted one ot the most abundant benthic invertebrates sampled in the lake. However, the high food overlap value noted, showing high similarity in their feeding habits, suggests that competition between the two species may be possible under certain circuinstances.
ACKNOWLEDGEMENTS

Although the mormyrid species studied herein belong to the same trophic guild (insectivorous fish), they exhibit some differences in their main prey items {P. bovei feeds mainly on chaoborid larvae whereas Marcusenius species preferentially select chironomid larvae). This segregation of food items may reduce interspecific competition and may allow the coexistence of P. bovei and Marcusenius species. Besides the segregation between main food items, P. hovei is a pelagic fish (De Merona 1980) whereas all other mormyrid species, including Mareusenius species live in the deep area of the river. This difference in habitat used by these sympatric mormyrid species may also contribute to the reduction of interspecific competition. In Marcusenius species, the use of the same main prey item was reflected in the high dietary overlap. Consequentiy, competition among these species is expected to be high (Greenberg 1991). But, at least three conditions are known to be necessary before competition occurs (Angermeier 1982): 1) critical resources must be in short supply; 2) the resources must be shared, and (3) the sharing must result in impaired reproductive

ALLAN, J.D. 1995. Stream Ecology: Structureand Function of Running Water!>. Chapman & Hall, London. ANCERMEIER, RL 1982. Resource seasonality.ind fish diets in an Illinois stream. Eiwirotwwiital Bioto'^ of Fishes 31: 389-401. ARRINGTON, D.A. WINEMILLER, K.O. LOFTUS, W.H & AKIN, S. 2002. How often do fishes 'run on empty'? 0%-!/83: 2145-2151. BIGORNE, R. 1990. Mormyridae. In: Fainw des poisons d'eaiix douces et saumatres de iAfrique de rOticst, (eds) C. Leveque, D. Paugy & G.G. Teugeb, Gollection Faune tropicale XXVIII, Tome 1, p p . 122-184. ORSTOM, Paris, and MRACTervuren. CHIMBARI, M.j. NDAMBA, .|. & MADSEN, H. 1996. Food selection behaviour of potentiai biological agents to control intermediate host snails of schistosomiasis: Sargochroniis codringtoni and Tilnpin rvndalii. Ada Tmpka 61(3): 1991-199. DEJOUX, C.J. ELOUARD, M. FORGE, R & MASLIN, l.L. \9?.\. Catalogue iconographiqtie des insedes aijiKitiqua dc Cotedlvoire. ORSTOM, Paris. DE MERONA, B. 19H(). Ecologie de Petrocepljalus bovei (Pisces, Mormyridae) dans les rivieres de Cote d'lvoire. Giiners ORSTOM, Serie H]/drolnolo>iie 13: 117-127. DIAMOND, J.M. 1970. Ecological consequences of island colonisation by Southwest Pacific birds. I. Types of shifts. Proceedings National Academy of Sciences USA 67: 529-536.

Kouamelan et al.: Resource partitioning among mormyrid fishes from Lake Ayame, Ivory Coast DIERL, W. & RING W. 1992. Cuidedes Insectes: Deseriptioi, Habitat et Moeiirs. Delachaux et Niestle, Neuchatel. OIOMANDE, D. & GOURENE, G. 2005. Premieres donnees sur la macrofaune benthique de I'hydrosysteme Huvio-Iacustre de la Bia (Cote d'lvoire). Science et Nature 2{2): 167-176. [STEVES, K.E. 1996. Feeding ecology of three Asti/anax species {Characidae, Tetragonopterinae) from a floodplain lake of Mogi-Guaiju River, Parana River Basin, Brazil. Environmentai Biolof^ of fishes 46: 83-UlL liSTEVES, K.E. & GALETTI, RM. 1995. Food partitioning among some characids of a small Brasilian floodplain lake from tiie Parana River Basin. Environmental BiolOgif of Fishes 42: 375-389. C;ARCIA-FRANOUESA, E. MOLINERO, A. VALERO, J. & FLOS R. 1996. Influence ot sex, age and season on the feeding habits of the flatfish Solea senegalensis. F.nvironmenlai Biology of Fishes 47: 289-298. t;iBSON, R.N. & HZZi/LA. 1987. Feeding relationships of a demersal fish assemblage on the west coast of Scotland, jmirnal of Fish Biohg}i 3: 55-69. ClOLDSCHMIDT, I WITTE, E & DE VISSER, J. 1991. Ecological segregation in zooptanktivorous haplochromine species (Pisces: Cichlidae) from Lake Victoria. Oikos 58: 343-355. GRAY, A.E. MULLIGAN, TJ. & HANNAH. R.W. 1997. Food habits, occurrence, and population structure of the hat ray, MyliohUis califoniica, in Humboldt Bay, Galifornia. Fnvironmeidnl Biology of Fishesi9:227-238. C.REENBERG, LA. 1991. Habitat useand feeding behavior of thirteen species of benthic stream fishes. rti>iromwntal Biology af Fishes 31: 389-401. liAjlSAMAE, S. CHOU, L.M. & IBRAHIM, S. 2003. Feeding habits and trophic organization of the fish community in shallow waters of an impacted tropical habitat. F.Aiiayine, Coastal und Shelf Science 58: 89-98. I lOPKINS, G.D. 1981. On the diversity of electric signals in a community of mormyrid electric fish in West Africa. Anicriean Zoologist 21: 211-222. I iORI, M. 1987. Mutualism and commensalism in a fish aimmunily in Lake Tanganyika. In: Ewhttian and Coadaptation in the Biotic Communities, (eds) S. Kawano, |.H. Connell & I Hidaka, pp. 219-239. University of Tokyo Press, Tokyo. HORN, H.S. 1966. Measurement of'overlap' in comparative ecological studies. The American Naturalist 100: 419-424. HUGUENY, B. GAMARA, S. SAMOURA, B. & MAGASSOUBA, M. 1996. Applying an index of biotic integrity based on fish assemblages in a West African river. HvdrolmMia 331:71-78. HUTCHINSON, G.E. 1965. The Ecological Theatre and the Evolutionary Play. Yale University Press, New Haven. HYSLOn E.J. 1980. Stomach contents analysis, a review of methods and their application. Journal of Fish Biology 17: 411^29. HYSLOR E.J. 1986. The food habits of four small sized species of Mormyridae from the floodplain pools of Sokoto Rima River basin, Nigeria. Journal of Fish B/('/tn,n/28: 147-151. KING. R.P. UDOIDIONG, O.M. EGWALI, E.C. & NKANTA, N.A. 1991. Some aspects of the b-ophic biology of llislta afrieana (Teleostei; Pristigasteridae) in

273

Qua Iboe estuary, Nigeria, journal of African Zoology 105:261-274. KONE, T 2tKK). Regime alimentaire et reproduction d'un titapia lagunaire [Sarotherodon melanoiheron RCippfll, 1852) dans la riviere Bia et le lac de barrage d'Ayamt^ (Cote d'lvoire). These de Doctorat, Katholieke Universiteit Leuven, Belgium. KOUAMELAN, E.R TEUGELS, G.G. GOURENE, G. OLLEVIER E & THYS VAN DEN AUDENAERDE, D.FE. 1999. The effect of a man-made lake on the diet of the African electric fish Mormyrus rume Valenciennes, 1846 (Osteoglossiformes; Mormyridae). Hydrolmlogia 380: 141-151. KOUAMELAN, E.R TEUGELS, G.G. GOURENE, G. THYS VAN DEN A U D E N A E R D E , D.F.E. & OLLEVIER, E 2000. Habitudes alimentaires de Mormyrops anguilloides (Mormyridae) en milieu lacustre et fluvial d'un basin Ouest Africain. Cybium 24(1): 67-79. LAUZANNE, L. 1983. Lake Chad. 15. Trophic relations of fishes in Lake Chad. Monographiae Biohgicae 53: 489518. LAUZANNE, L. 1988. Les habitudes alimentaires des poissons d'eau douce afdcains. In: Biologie et ecologie des poissons d'eau douce Africain^, (eds) C. Leveque, M.N. Bruton & G.W. Ssentongo, pp. 221-242. ORSTOM, Paris. LEVEQUE, C. 1997. Biodiversity Dynamics and Conservation: the freshumter Fish of Tropical Africa. Cambridge University Press, Cambridge. MACDONALD, WW (1956). Observations on the biology of chaoborids and chironomids in Lake Victoria and on the feeding habits of the elephant snout fish [Mormxfrus kannume Forsk.). jounal of Animal Eeoio-^y 25: 36-53. MARSHALL, S. & ELLIOTT, M. 1997. A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific feeding relationships in estuarine fish. }ourml offish Bwlogij 51: 526-545. MARTIN, ED. 1984. Diets of four sympatric species of Etheolstoim (Pisces: Percidae) from southern Indiana: interspecific and intraspecific multiple comparisons. Environmental Biology of fishes 31: 113-120. MOORE, J.W & MOORE, LA. 1976. The basis of food selection in flounders, Platichthys flesus (Linnaeu) in Severn Estuary, journal of Fish Biologi/t: 139-156. MORISITA, M. 1959. Measuring of interspecific association and similarity between communities. Memoirs of the Faculty of Sciences. Kyushu University. Sfr, E {Biologi/): 65-80. NATARAJAN, A.V & JHINGRAN, A.G. 1961. Index of preponderance - a method of grading the food elements in the stomach analysis of fishes. Indian lournal of Fisheries 8: 54-59. ROOT, R.B. 1967. The niche exploitation paltern of the bluegray gnatcatcher. Ecolo'^ieal Mono-Graphs 37: 317350. ROSECCHI, E. & NOUAZE, Y. 1987. Gomparaison de cinq indices utilises dans l'analyse des contenus stomacaux. Revue ties TravaiLx de I'lnstitut de Peches Maritimei9: \U-123. ROSS, S. 1986. Resource partitioning in fish assemblages: a review of field study. Copeia 2: 352-388.

274

African Zoology Vol. 41, No. 2, October 2006 ing habits of Haplochromis (Teleostei: Cichbdae) from lake Kivu in Africa, I. Interspecific relations. Belgian journal ofZixilo'^j 120:143-155. VANDEN BOSSCHE, J.P & BERNACSEK, G.M. 199(1. Source Book for the Inland Fishery Resources of Africa. FAO Fisheries Technical Paper 18/2, Rome. WINDELL, JT. & BOWEN, S.H. 1978. Methods for study of fish diets based on stomach contents. In: Mctlmh for Assessment of Fish Production in Freshwater, (ed.) J. Bagenal, 3rd edn, pp. (X)-00. Blackwell Scientific Publications, Oxford. WITTE, E 1984. Ecological differentiation in Lake Victoria haplochromines: comparison of cichlid species flocks in African Lakes. In: Ex'olufion of Fish SpcitfsF/offo, (eds) A.A. Echelle&I.L. Kornfieldn, pp, 155-167. Oklahoma State University Press, Stillwater. ZARET, TM. & RAND, A.S. 1971. Competition in tropical stream fishes: support for the competitive exclusive principle. Ecology 52: 336-342.

SCHOENER,TW. 1974. Resource partitioning in ecological communities. Science 185: 27-39. SCR]MGEOUR,G.J. & WINTERBOURN, M.J. 1987. Diet, food resource partifioning and feeding periodicity of two riffle-dwelling fish species in New Zealand River. journal of Fish Biology 53: 309-324. SIMENSTAD, C.A. 1979. Fish food habits analysis. Principal Investigation Report and Assessment of Alaskan Continental Shelf: 441-150. SNOW, B.K. & SNOW, D.W. 1972. Feeding niches of hummingbirds in a Trinidad valley, journal ofAninm! Eco/o^sT/41: 471-486. TAYLOR, J. 1984. Comparative evidence for competition between the salamanders Ambx/stoma gracile and Tariclm granulosa. Copeia 3: 672-683. TOFT, C.A. 1985. Resource partitioning in amphibians and reptiles. Copeia 1: 1-20. ULYEL, A.P OLLEVIER, E THYS VAN DEN AUDENAERDE, D.EE. & CLUSTERS, R. 1990. Food and feed-