Journal o f Fish Biology ( 1991) 39, 15-24

The diet of lidole (Trewavas) and other chambo species in Lakes and Malombe

G . F. T u r n e r * } , A. S. G rim m * , O. K . M H O N E f, R. L. Robinson*§ and T. J. P i t c h e r * || * School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, U.K. and+Cape Maclear Fisheries Research Station, P.O. Box 27, Monkey Bay, Malawi

(Received8 June 1990, Accepted8 January 1991)

Oreochromis lidole (Trewavas) is a member of a flock of tilapiines endemic to the catchment area, of which it is considered to be the most pelagic and planktivorous species. Analysis of the stomach contents of adults from the South East Arm of Lake Malawi, from fish caught by both the offshore trawl fishery, and the inshore gillnet fishery, indicates a very narrow dietary breadth, dominated by the filamentous Melosira. The presence of quantities of sand in the stomach indicates that at least some of the food is obtained from sediment feeding. During the breeding season, in November, brooding female O. lidole caught in shallow water exhibited a much broader diet, resembling the more inshore species O. squamipinnis (Gunther) and 0. karongae (Trewavas), with a higher proportion of filamentous chlorophytes and a large amount of sand. Juvenile chambo initially feed mainly on epilithic and epiphytic , turning more to and sediment at larger sizes. In general, the different Oreochromis spp. caught in the same place at the same time have very similar diets, suggesting that any avoidance of competition for food resources results from habitat partitioning.

Key words: Oreochromis', Lake Malawi; diet; algae.

I. INTRODUCTION

The of the African Great Lakes represent the largest extant vertebrate species flocks, probably comprising over 1000 species, an unparalleled diversity which demands explanation by evolutionary biologists. Particularly striking is the diversification of feeding structures (jaws, teeth and pharyngeal bones), believed to be associated with the adoption of specialized diets (Fryer & lies, 1972). How­ ever, McKaye & Marsh (1983) observed food switching in two morphologically specialized Lake Malawi haplochromine cichlids, while Reinthal (1987) found considerable overlap in the diets of rock-dwelling Malawian species. While there are perhaps as many as 600 morphospecies of haplochromine cichlids in Lake Malawi, only six tilapiine species have been described from the lake, but these too show morphological specializations in feeding structures, which have been regarded as indications of dietary specialization (Lowe, 1952). rendalli Boulenger, a species widely distributed throughout Africa feeds on macro- phytes. Oreochromis (Oreochromis) shiranus (Boulenger) is an inshore-dwelling benthic feeder. The other species, comprise a monophyletic flock (Trewavas, 1983)

t Present address: FAO Chambo Fisheries Project, Monkey Bay Fisheries Research Station, P.O. Box 27, Monkey Bay, Malawi. ^Present address: Department of Parks and Wildlife, P.O. Box 27, Monkey Bay, Malawi. KPresent address: Renewable Resources Assessment Group, Centre for Environmental Technology, Imperial College of Science, Technology and Medicine, 8 Princes Garden, London SW1 1NA, U.K. 15 0022 1112/91/070015+10 $03.00/0 © 1991 The Fisheries Society of the British Isles 16 G. F. TURNER

T able I. Samples collected for qualitative analysis

Locality Habitat type Period n Class/species

Cape Maclear Rocky, shallow Apr.-Dec. 1989 260 Juveniles (Domwe Is.) Cape Maclear Sand, shallow Apr.-Dec. 1989 280 Juveniles (Msaka) Cape Maclear Rocky/sandy, shallow Nov. 1988-Jan. 1990 340 Juveniles Cape Maclear Rocky/sandy, shallow Nov. 1988-Jan. 1990 282 Adults Cape Maclear Rocky/sandy, shallow Oct. Dec. 1989 47 Nesting males Cape Maclear Rocky/sandy, shallow Nov. 1989 4 O. lidole fry SE Arm Sandy/muddy, deep Dec. 1988-Dec. 1989 243 Adults (offshore) Lake Malombe Muddy, shallow Oct. 1989-Dec. 1989 99 Adults

of the subgenus Nyasalapia, known as ‘ chambo Lowe (1952) considered that of this group, O. lidole (Trewavas) was the most pelagic species, and suggested that on the basis of its streamlined body shape, reduced dentition and narrow pharyngeal bone, that it was a specialized phytoplankton feeder. O. karongae (Trewavas) [formerly O. saka (Lowe), Turner & Robinson, 1991] which has heavier dentition and a wider pharyngeal bone, and the intermediate O. squamipinnus (Gunther) were believed to be more benthic in their habits and diets. As part of a wider study on the biology of O. lidole, we here examine the diet of this species, and its relatives, to ascertain the importance of planktonic and benthic feeding and the degree of dietary specialization in the species flock.

II. METHODS

SAMPLING Qualitative analysis of stomach contents of chambo was carried out at Cape Maclear Fisheries Research Station (Table I) using a low power microscope. Positive identification of juveniles is not yet possible, and methods for identifying adults time-consuming (Turner et al., 1989). For these reasons, data from these large samples could not generally be broken down by species, but more detailed analyses were performed on 108 stomach contents returned to Bangor (Table II). after preservation in Lugol’s Iodine. In these cases, the species of the chambo was determined by external body measurements (Turners/ al., 1989) and dissection and examination of the lower pharyngeal bone (Trewavas, 1983). For analysis of seasonal variation, samples of adult O. lidole were collected from the commercial trawl fishery in the South East Arm of Lake Malawi, where they could most reliably be obtained year-round. During the months of September and October, adult 0 . squamipinnis were also frequent in the catch, and both species were sampled in this period, to determine the degree of dietary overlap between these species when found offshore. During its breeding season, which peaks from October to November, adult O. lidole come inshore to breed on clean sandy and rocky beaches (Lowe, 1953), while females brood the fry in a variety of habitats, including more eutrophic areas. Thus the month of November was chosen to sample O. lidole in a variety o f areas to determine its dietary flexibility, while the other Oreochromis species were also sampled at this time to assess the degree of overlap between the diets of all species. Chambo were sampled from Cape Maclear (Fig. 1) a clean sandy/rocky area which is a known O. lidole breeding site (Lowe, 1953), and from Lake Malombe, a shallow eutrophic lake connected by a short stretch of river to the extreme DIET OF OREOCHROMIS LID O LE 17

T a b le II. Samples collected for quantitative analysis

Locality Habitat type Period n Species

SE Arm Sandy/muddy, deep Feb. and Sep.-Dee. 1989 40 0 . lidole (offshore) SE Arm Sandy/muddy, deep Sep. Oct. 1989 16 0 . squamipinnis (offshore) SE Arm Sandy, shallow Nov. 1989 8 0 . lidole (inshore) Cape Maclear Rocky/sandy, shallow Nov. 1989 8 0 . lidole Cape Maclear Rocky/sandy, shallow Nov. 1989 8 0. karongae Cape Maclear Rocky/sandy, shallow Nov. 1989 8 O. squamipinnis Lake Malombe Muddy, shallow Nov. 1989 8 0 . lidole Lake Malombe Muddy, shallow Nov. 1989 8 0. karongae

F ig . 1. Southern Lake Malawi and Lake Malombe, showing the localities where chambo were collected.

southern tip of Lake Malawi, a locality where 0 . lidole females brood young, but do not spawn. For comparison with the offshore-caught fish, a sample of O. lidole was obtained by gillnetting at Mpemba in the South East Arm in November 1989. Underwater observations were made of the feeding behaviour of juvenile, and where possible, adult chambo, at Domwe Island, West Thumbi Island and Chembe beach. In July 1988, the feeding sites of some 638 chambo were recorded underwater at West Thumbi island. These fish were classed into four groups, by size, which was estimated after compari­ son of size estimates made underwater with fish subsequently netted and measured.

ANALYSIS The stomachs o f 1555 chambo were examined at the Cape Maclear Field Station, using a low power microscope. Five fields were scanned and note was made of the dominant algal genus, and the presence or absence of other taxa. 18 G. F. TURNER

100

G 3 * o

5-7 8-12 13-17 17 S.l. fish (cm )

Fig. 2. Proportions of chambo of various size classes feeding on different resources at West Thumbi Island. ■ , Plankton; E, sediment; n,epiphyton; 01, epilithon.

Of the samples returned to Bangor for detailed analysis, between 200 and 500 cells or colonies were counted from each stomach (eight stomachs for each fish species/locality/ month). Individual cells were counted for genera with large cells, such as Melosira, Cladophora and Spirogyra. For other colonial taxa, the number of colonies was counted. Thus, in figures used for percentage occurrence, Melosira, for example, is represented by individual cells, while Mougeotia is the number of filaments, a sample of 10-20 cells or colonies of each algal taxon was measured, and from this information figures for percentage composition by volume were calculated. For cyanophytes possessing a gelatinous sheath, only the cellular volume was calculated. Zooplankton was found in a number of stomachs, but was excluded from the calculations of percentage volumes, as its patchy occurrence and large volume would lead to large sampling-induced variation in the results. Algae were identified to generic level, where possible, but in some cases (e.g. Microcystis) several distinct forms of one genus were found to have clearly different distributions or cell volumes. These were scored separately, and regarded as separate taxa for further calculations. Dietary breadths were calculated from the mean sample percentage volume or percentage occurrence using Levins’ Index (Levins, 1968):

I i Iph where p j is the proportion of algal taxon i in the diet o f the sample. Dietary overlaps were calculated from data on both percentage occurrence and percentage volume, using Schoener’s Index (Linton etal., 1981):

l - d ( P ff- ^ ) / 2 ) ; where p jf is the proportion of algal taxon i is the diet of fish j and p ik is the proportion of taxon i in the diet o f fish k. This was used to show variation within a species collected in the same place at the same time, by calculating the mean within-sample overlap, as well as for the comparison of species and localities, which was carried out on the mean sample proportions. To assess the importance of benthic feeding in the diet, the percentage volume of sand in the stomach was estimated by low-power microscopic examination of the sample.

III. RESULTS FEEDING SITES Underwater observations showed that the smallest juveniles fed principally on encrusting algae growing on rocks and macrophytes (Fig. 2). At larger sizes, plankton and sediment became more important sources of food. Analysis of stomach contents of juveniles revealed that a high proportion contained benthic DIET OF OREOCHROMIS LIDOLE 19

T a ble III. The diet, expressed as percentage of stomachs, of unidentified chambo species from Lake Malawi and Lake Malombe

Juveniles Adults ( > 17 cm s.l .) Dominant taxon Cape Maclear Cape Maclear SE Arm Lake Malombe (n = 880) (m = 282) (« = 243) (m = 99)

Melosira 8-0 15-2 8 6 0 8-1 Mougeotia 85-1 75-2 12-3 91-9

Anabaena 6-9 9-6 — —

Taxon present Benth. Cyan.* 27-4 8 0 5-4 5-1 Benth. Chlor.t 261 8-9 7-9 5-1 Crustacea 80 160 14*0 16-2

‘ Benth. Cyan., attached filamentous benthic cyanophytes (mainly Calothrix). tBenth. Chlor., attached filamentous benthic chlorophytes (mainly Cladophora and Spirogyra). filamentous genera, both Chlorophytes and Cyanophytes (Table III). The pro­ portion of stomachs containing attached benthic species was much less for adult fish at all localities. The proportion of sand grains in the stomach varied according to locality, species and season (Table IV), being generally lower among O. lidole than sympatric specimens of the other species, and high among all fish taken at Cape Maclear. This suggests that O. lidole feeds to a greater extent on plankton rather than sediment as the other species do.

COMPONENTS OF DIET Of the adult chambo collected at Cape Maclear (Table III), all contained large amounts of a filamentous chlorophyte, and a filamentous cyanophyte (tentatively identified as Mougeotia and Limnothrix respectively, H. Bootsma, pers. comm.), various small , as well as globular cyanophytes. The latter, although abun­ dant, consisted largely of mucilaginous capsule, and did not contribute greatly to the overall cellular volume. Melosira was usually present in large quantities, but was only the dominant taxon in August and September. Anabaena dom inated the stomach contents of many fish in January and December, but was otherwise rare. The diet of juveniles at Cape Maclear (Table III) was essentially similar to that of adults, apart from the greater frequency of benthic attached species. Melosira was dominant mainly during a bloom in July 1989 which occurred simultaneously at the Msaka and Domwe sampling sites (there were no notable differences between the diets of fish caught at these two sites, and so the data have been combined). Examination of the stomach contents of four juvenile O. lidole taken from the mouths of brooding females caught on Chembe beach showed that their diet was dominated by Mougeotia. Globular cyanophytes, the planktonic chlorophyte Pediastrum, the benthic chlorophyte Cladophora and a stalked ciliate protozoan were also found, and one contained quantities of sand, suggesting both sediment and plankton feeding. Adult chambo caught offshore in the SE Arm of Lake Malawi (Table III), contained mostly Melosira. Mougeotia and Limnothrix were present in most 20 G. F. TURNER

T a ble IV. Dietary breadths and mean within-group dietary overlaps for Oreochromis spp. in Lakes Malawi and Malombe

Species and Dietary Mean within-group Month % Sand locality breadth diet overlap

O. lidole SE Arm Feb. 1-04(1-34) 0-99(0-92) 11-3 (offshore) Sep. 1-07 (1-21) 0-99 (0*95) 15-0 Oct. 1-03(1-14) 0-98 (0-94) 10-5 Nov. 1-04(1-14) 0-99 (0-93) 3-8 Dec. 2-60 (3-62) 0-76 (0-73) 13-0 SE Arm Nov. 1-08(1-35) 0-98 (0-87) 10 (inshore) Cape Maclear Nov. 5-94 (2-44) 0-58 (0-77) 55-0 Lake Malombe Nov. 2-67 (3-50) 0-49 (0-52) 2-0

0. squamipinnis SE Arm Sep. 107(110) 0-98 (0-96) 75-0 (offshore) Oct. 1 06 (110) 0-96 (0-94) 31-3 Cape Maclear Nov. 3-77 (6-73) 0-62 (0-60) 81-3

0. karongae Cape Maclear Nov. 7-08 (5-28) 0-48 (0-57) 89-8 Lake Malombe Nov. 2-64(5-08) 0-49 (0-52) 33-3

F'igures are calculated from values for percentage volume and, in parentheses, percentage frequency. Also shown is the mean percentage of sand, by volume, in the stomachs. stomachs, but were seldom the dominant taxa. remains were frequent. Fish remains were found in several chambo, in one case it was possible to identify them as being of Engraulicypris sardella (Gunther), a pelagic cyprinid. Adults from Lake Malombe contained a diverse mixture of Mougeotia, Melosira, Limnothrix, small diatoms, globular cyanophytes (Gloeocystis or Chroococcusl), Anabaena, fragments of Calothrix, Peridinium and crustacean remains. The first two of these were usually most abundant (Table III). Dissection of 47 (43 O. karongae and four O. lidole) adult males caught on or near their nests by Scuba diving, showed that the guts were entirely empty. Examination of male O. squamipinnis from Domwe Island and Lake Malombe, indicated that all males which were running ripe (i.e. it was possible to produce a flow of milt by squeezing the abdomen) had empty guts, while other males in breeding dress, but not running ripe, had full stomachs. The reason for this breed­ ing fast is unclear, as in m any localities, territorial male cham bo leave their nest for long periods of the day, and reproduction seems to be largely confined to the early morning (Turner et al., 1991). The nesting areas were not unsuitable for foraging: female and juvenile fish were often seen actively feeding in the vicinity o f a chambo nest.

DIETARY BREADTH From the detailed analysis of 52 stomachs of chambo of known species, it is apparent that dietary breadths for percentage volume (Table IV) were narrower in DIET OF OREOCHROMIS LID O LE 21

T a b le V. Seasonal variation in diet

Species Locality Months compared Dietary overlap

0 . lidole SE Arm Feb./Sep. 0-97 (0-89) (offshore) Sep./Oct. 0-98 (0-97) Oct./Nov. 0-99 (0-88) Nov./Dec. 0-60 (0-26) 0. squamipinnis SE Arm Sep./Oct. 0-99 (0-99) (offshore)

Resource use overlaps between successively-sampled months for offshore-caught O. lidole and O. squamipinnis. Figures are calculated from values for percentage volume and, in parentheses, percentage occurrence.

T a ble VI. Dietary overlaps between populations of O. lidole sampled in November 1989

SE Arm (inshore) 0-97 (0-88) Cape Maclear 0-20 (017) 0-21 (0-09) Lake Malombe 0-49 (0-40) 0-49 (0-30) 0-50(0-32) SE Arm SE Arm Cape Maclear (offshore) (inshore)

Figures are calculated from values for percentage volume, with percentage occurrence in parentheses. fish caught in the SE Arm (range: 1 03-2-6) than Cape Maclear (range: 3-77-7-08) or Lake Malombe (range: 2-64-2-67). Dietary breadths for percentage occurrence do not show such a clear pattern. Within the SE Arm, dietary breadths were approximately the same for O. lidole and O. squamipinnis caught in the same months and for inshore- and offshore-caught O. lidole from November. In Lake Malombe and at Cape Maclear, all species exhibited wide diet breadths (Table IV).

RESOURCE OVERLAP WITHIN SPECIES Figures for the mean dietary overlaps between members of the same species caught in the same locality in the same months are given in Table IV. Within-group dietary overlaps are high for SE Arm fish, but low for others. There was little variation between the diets in successively-sampled months for offshore-caught fish (Table V), apart from the relatively low overlap between November and December for O. lidole. Inshore- and offshore-caught O. lidole from the SE Arm show a high degree of similarity in their diets (Table VI). Possibly these are samples of the same population of fish, being caught offshore during the day by trawlers, and inshore at night by gillnets, as a result of a shorewards migration in the evening. Cape Maclear and Lake Malombe samples of O. lidole taken in November show very little similarity in their diets to SE Arm fish, or to each other. 22 G. F. TURNER

T a b le VII. Dietary overlaps between species of Oreochromis

Cape Maclear Nov. 0. squamipinnis 0-58 (0-70) O. karongae 0-69(0-46) 0-64(0-57) O. lidole O. squamipinnis

SE Arm, offshore O. lidole/O. squamipinnis Sept. 0-99 (0-95) 0 . lidole/O. squamipinnis Oct. 0-98 (0-96)

Lake Malombe, Nov. 0. lidole/O. karongae 0-49 (0-40)

Figures are calculated for data from percentage volume, and in parentheses, percentage occurrence.

Principal Component I

F ig . 3. Plot of the first two principle components from analysis conducted on the percentage volumes of 33 algal taxa taken from stomachs of chambo collected in October and November 1989. Minimum convex polygons are drawn to enclose all data points. SE Arm includes O. squamipinnis caught offshore in October and O. lidole caught offshore in October and November, and inshore in November.

RESOURCE OVERLAP BETWEEN SPECIES Dietary overlaps between the species caught in the SE Arm were high (Table VII), and much lower at Cape Maclear and in Lake Malombe. However, this pattern is probably a reflection of individual variation and diet breadth, rather than a true indication of greater dietary specialization occurring at Cape Maclear DIET OF OREOCHROMIS LID OLE 23 and Lake Malombe. For example, the mean between-species dietary overlap by volume at Cape Maclear is 0-64, while the mean within-species overlap is 0-62. The figures for the SE Arm in September and October are 0-99 and 0-98 respect­ ively. Thus all fish irrespective of species have similar diets in the SE Arm, while there is great individual variation at Cape Maclear and Lake Malombe. Principal Components Analysis carried out on mean percentage volumes of 33 algal taxa from stomachs collected in October and November shows how consider­ able is the change in the diet of O. lidole as it moves from offshore in the SE Arm to the shallow waters o f Cape M aclear (Fig. 3). O. squamipinnis alters its diet to a much lesser extent, and shows greater variation. The dietary shift by O. lidole entering Lake Malombe is much less marked, although it becomes more similar to the resident O. karongae.

IV. DISCUSSION

The results demonstrate that locality is the most important source of variation in the diet of O. lidole and its relatives, and that differences between specimens of different species caught in the same place at the same time are negligible and are probably the result of individual variation in diet. It appears that differences in morphology of feeding structures do not contribute to the avoidance of competition between sympatric members of the different species, but perhaps can be seen as a reflection of differential habitat use, which results in differences in the availability of different food sources. When the species occupy the same habitat they eat the same things, but distribution between habitats varies between the species. An accurate measure of dietary overlaps between the species would have to take account o f the relative times spent in the different habitats by individuals of each species. In a similar analysis, Reinthal (1987) found instances of high dietary overlaps (up to 0-86) between different species of mbuna (rock-dwellng haplochromine cichlids) in the Cape M aclear area of Lake M alawi, and in a more qualitative study Fryer (1959) reported similar results. Ribbink et al. (1983) suggest that these similarities may be deceptive, since different species may obtain the same algal species from different parts of the habitat—for example, while Labeotropheus fuelleborni Ahl was found to feed mainly from the upper surface of rocks, the sympatric sibling species L. trewavasae Fryer fed mainly from the lower surfaces. These findings suggest that the different chambo species may feed in different microhabitats, which is consistent with the differences in the amount of sand found in the stomachs of O. lidole and O. squamipinnis taken from the SE Arm. Underwater observations on the feeding behaviour of the different species would perhaps clarify the situation, but our attempts to do so were frustrated by the difficulty in identifying the juveniles in the field, and the extreme wariness of adults towards divers.

The study formed part of the Overseas Development Administration Lidole Project, Grant R4334. We thank the Malawi Government for permission to carry out this research and the Malawi Fisheries Department for providing the facilities of the Cape Maclear Field Station. We thank H. Bootsma for advice on algal identification. Particular thanks are due to G. Kamanga, C. Katunga, T. Mhango, J. Mtawali, J. Smart and J. Witimani for technical help in Malawi. We thank the staff of the Monkey Bay Fisheries Laboratory and 24 G. F. TURNER

FAO/Malawi Government Chambo Project, in particular S. B. Alimoso, J. Magasa, L. M. Phiri, M. Seisay, D. Tweddle and N. P. van Zalinge for their co-operation in many practical matters and unforeseen emergencies.

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