Biological Journal o f the Linnean Society (1985), 25: 331 -338

Feeding-site utilization in three sympatric species of (Pisces, Cichlidae) from

A. C. MARSH*

Department o f Zoology, University o f the Witwatersrand, Johannesburg 2001, South Africa

AND

A. J. RIBBINK

J.L .B . Smith Institute o f Ichthyology, Private Bag 1015, Grahamstown 6140, South Africa

Accepted fo r publication November 1984

Three sympatric sibling species of Petrotilapia, with similar dietary and macrohabitat requirements, occur near Monkey Bay, Lake Malawi. Males and females of all three species fed selectively on the rocky shores. Males utilized less than 6% of the space they defended as a breeding territory for feeding and although interspecific overlap of territories was considerable, only 2.5% of the feeding space used by territorial males was shared. Males primarily utilized rich food patches which occurred within the territories of highly aggressive Pseudotropheus species, whereas females tended to feed in undefended areas. Although Petrotilapia species are not highly aggressive fishes, there was a well-defined social dominance hierarchy amongst them and it is suggested that feeding-site utilization is dependent on social rank. Inter- and intraspecific differences in feeding-site utilization probably facilitate species coexistence and thus contribute to the maintenance of the high species diversity which is a characteristic of the ichthyofauna of Lake Malawi.

KEY WORDS:— Ecology - diversity - species persistence - coexistence - microhabitat utilization - competition - social dominance - sibling species.

CONTENTS

I n tr o d u c tio n ...... 331 M aterials and m ethods...... 332 R e s u l t s ...... 333 D iscussion...... 336 A c k n o w le d g e m e n ts ...... 337 References...... 337

INTRODUCTION The Great Lakes of Africa contain speciose fish faunas which are dominated by the Cichlidae and which have evolved in a short time (Fryer & lies, 1972;

•To whom all correspondence should be addressed. 331 0024-4066/85/080331 4-08 $03.00/0 (g) 1985 The Linnean Society of London 332 A. C. MARSH AND A. J. RIBBINK Greenwood, 1974). For example, Lake Malawi, which is only about two million years old (Dixey, 1926; Fryer, 1959; Greenwood, 1974; Banister & Clarke, 1980), has almost 300 described endemic species of and it is estimated that a further 200 species await description (Ribbink et al., 1983). A knowledge of species formation and persistence is a prerequisite for understanding the high species diversity encountered in these lakes (Lowe-McConnell, 1969). Species persistence is primarily an ecological problem, one of its essential components being the coexistence of sympatric species. To comprehend the manner and extent of differences in morphology and habit among closely related sympatric species is essential to an understanding of coexistence and hence diversity (Schoener, 1974). The rocky shores of Lake Malawi are dominated by a group of closely related known collectively as Mbuna (Fryer, 1959; Ribbink, Marsh, Marsh, Ribbink & Sharp, 1983). The Mbuna contain a number of sympatric sibling species complexes (Holzberg, 1978; Marsh, Ribbink & Marsh, 1981; Ribbink el al., 1983) which, by definition, are closely related and have very similar or identical morphologies (Mayr, 1963). Since it is likely that closely related species have similar ecological requirements, problems of coexistence are likely to be highlighted in sibling species complexes. This study focuses on three sympatric sibling species of Mbuna belonging to the genus Petrotilapia. Previous work has shown that the three species, in the vicinity of Monkey Bay (14° 03'S, 34° 55'E), appear to have very similar dietary and spatial requirements (Marsh et al., 1981; Marsh, 1983; McKaye & Marsh, 1983; Ribbink et al., 1983). Sharp (1981) found that Petrotilapia territorial males appear to feed primarily within the territories of two highly aggressive, undescribed Pseudotropheus species: P. elongatus ‘aggressive’ and P. tropheops ‘orange chest’ (throughout this manuscript we have used the informal names from Ribbink et al. (1983) for these undescribed species). Furthermore, Sharp (1981) showed that the territories of P. elongatus ‘aggressive’, the more aggressive of the two Pseudotropheus species, support approximately 2.25 times more epilithic algae than similar undefended sites, with larger individuals occupying larger and more productive sites than smaller individuals. Similarly, P. tropheops ‘orange chest’ territories support approximately 1.6 times more epilithic algae than undefended sites. Thus, abundance of epilithic algae varies spatially and the richer the food patch the less accessible it is to most Mbuna in view of the aggression of the tenant of the food patch (= territory). These differences in food abundance and availability could form the basis upon which the Petrotilapia species partition feeding space. Here we show that there are interspecific and intraspecific differences in feeding-site utilization and aggression. It is suggested that the feeding sites are partitioned amonst the Petrotilapia individuals according to their position in a social dominance hierarchy.

MATERIALS AND METHODS The study took place on the northern and eastern shores of the island of Thumbi East, Monkey Bay, where rocky habitats extend down to a sandy bottom at 30-35 m. The nature of the rocky substratum varies but most areas comprise a rubble of rocks and boulders, ranging in diameter from 0.3 to 2 m, with very large flat rock slabs occurring at irregular intervals. Rock surfaces are covered by a thin mat of algae. FEEDING SITES OF PETRO TILAPIA 333 The following method was used to obtain information on feeding site utilization at the species level. Whenever an adult Petrotilapia was seen feeding, the feeding site was classified into one of four categories: (1) territories of P. elongatus ‘aggressive’ individuals > 100 mm t l , (2) territories of P. elongatus ‘aggressive’ individuals < 100 mm t l , (3) territories of P. tropheops ‘orange chest’, and (4) undefended areas. Feeding-site niche breadths were calculated using the formula W = r® (Petraitis, 1979), where r is the number of feeding-site categories sampled and r E - pij logr q3~ £ pj logrpij, . J=] w here p i} is the frequency with which a particular Petrotilapia form used one of the four feeding sites and q is the frequency of occurrence of a particular feeding-site category in the environment (data for q were obtained from Sharp, 1981). To obtain detailed information on the utilization of feeding space by territorial individuals, an area 12 x 10 m was divided into cells 50 x 50 cm, using nylon cords laid across the rocks, and the position of a fish could accurately be assigned to a cell of 25 x 25 cm. Each territorial male Petrotilapia that occurred within the grid was observed for a total of 6 h over a period of 10 consecutive days during May 1979, and its territory boundary and feeding sites were mapped. Once a month during 1980 eight randomly selected territorial males of each species were observed continuously for 15 min each between 08.00 and 10.00 hours in 1-5 m depth. Aggressive encounters between these males and other Petrotilapia individuals were observed to determine which fish was dominant in each encounter. Like most cichlids, Petrotilapia species possess a stereotyped agonistic behavioural repertoire involving the use of ‘lateral displays’, ‘tail beating’, ‘flank biting’ and ‘mouth fighting’ (terms after Baerends & Baerends van-Roon, 1950). Typically subordinant Petrotilapia individuals fled when challenged and the latter three behaviours were seldom evident. During agonistic displays dominant males intensified their livery, while subordinant individuals frequently adopted a duller coloration. Thus, it was a relatively simple matter to decide which protagonist was dominant. Laboratory experiments were performed to supplement the field observations. Territorial male Petrotilapia were placed, with a few Psuedolropheus zebra individuals, in 280 1 glass aquaria on either side of an opaque partition. Each aquarium always held two species of Petrotilapia and because there are interspecific differences in the size of mature males in nature (Marsh et al., 1981), no attempt was made to match the protagonists for size. Once the Petrotilapia males had established dominance over the P. zebra, and developed the intense coloration associated with territoriality in nature, the partition was removed and the responses of the two Petrotilapia males were noted. Similar experiments involving Petrotilapia males and P. elongatus ‘aggressive’ and P. tropheops ‘orange chest’ were also performed.

RESULTS

X2 tests, using the occurrences of the different feeding-site categories as the expected values, indicate that all Petrotilapia forms fed selectively {P < 0.001; 17 334 A. C. MARSH AND A. J. RIBBINK T able 1). Petrotilapia tridentiger males fed selectively in the territories of P. elongatus ‘aggressive’, especially favouring those held by large individuals; they utilized other feeding sites much less than expected. All other Petrotilapia forms utilized the territories of large P. elongatus ‘aggressive’ individuals much less than expected. Petrotilapia genalutea males, P. nigra males and P. tridentiger females fed selectively in the territories of small P. elongatus ‘aggressive’ individuals and those of P. tropheops ‘orange chest’, and fed less than expected in undefended sites. Petrotilapia genalutea females utilized P. tropheops ‘orange chest’ territories in proportion to their abundance, utilized other territories considerably less than expected and utilized undefended areas more than expected. Petrotilapia nigra females exhibited positive selection for P. tropheops ‘orange chest’ territories, utilized undefended sites in proportion to their abundance and other territories less than expected. Territorial males of all three species had narrower feeding- site niches than females. The narrowest niche was held by P. tridentiger males, with female P. genalutea and P. nigra occupying the broadest feeding niches (T able 3).

Table 1. Percentage frequency of feeding-site utilization and the factor (/) by which this differs from that expected if feeding sites were utilized in proportion to their abundance (+ / = site used f times more than random, —f = site used/tim es less than random)

Category of feeding site

Large P. agg. Small P. agg. P. troph. Undefended

Petrotilapia form % (/) % if) % (/) % (/) JV

P. tridentiger M 64 (+5.1) 24 ( + 3.2) 6 (-1.6) 6 (-11.8) 181 P. genalutea M 4 ( - 3 .1 ) 29 ( + 3.9) 29 ( + 3.1) 38 ( - 1.9) 183 P. nigra M 4 (-3.1) 21 ( + 2.8) 45 ( + 4.7) 30 (- 2.4) 220 P. tridentiger F 4 ( - 3 .1 ) 23 ( + 3.1) 20 ( + 2.1) 53 ( - 1.3) 192 P. genalutea F 0 ( - o o ) 1 ( - 7 .5 ) 10 (+ 1 .1 ) 89 ( + 1.3) 145 P. nigra F 0 ( - o o ) 5 ( - 1 .5 ) 15 (+ 1 .6 ) 80 ( + 1.1) 140

Large P. agg. = P. elongatus ‘aggressive’ individuals > 100 mm t l . Small P. agg. = P. elongatus ‘aggressive’ individuals < 100 mm t l . P. troph. = P. tropheops ‘orange chcst’. M — male, F — female.

Corroboration that Petrotilapia species utilize feeding sites selectively comes from the study of space utilization of nine Petrotilapia territorial males (six P. nigra, two P. tridentiger, one P. genalutea), which occurred within the grid. Relatively little of the area each male defended against conspecific males was used for feeding. Petrotilapia tridentiger, P. nigra an d P. genalutea males only used 3.2%, 4.3% and 5.9% of their territories, respectively, for feeding (data for P. tridentiger and P. nigra are means). Furthermore, although up to 22 feeding sites were used by any one male over the 10 day observation period, the majority of feeding took place in relatively few of these sites. During any one day most feeding movements, for any particular male, occurred in one or two sites only. Although interspecific overlap of territories was high, overlap of feeding space amongst territorial males was very low. O f the total feeding space FEEDING SITES OF PETROTILAPIA 335 utilized by these males only 2.5% was shared and simultaneous utilization of a feeding site was not recorded.

Table 2. Aggresive interactions between territorial male Petrotilapia at Monkey Bay. The data represent the total number of encounters in 60 h. Differences between all species pairs are significant {P < 0.001, X2 test)

Submissive

Dom inant P. tridentiger P. genalutea P. nigra

P. tridentiger 16 19 15 P. genalutea 0 26 8 P. nigra 0 1 15

Under natural conditions there were relatively few overt interactions between territorial males of the three species (Table 2). Of those that were observed, P. tridentiger consistently dominated P. genalutea and P. nigra territorial males. Of nine encounters between the latter two males, P. genalutea was dominant in all but one. In the laboratory experiments territorial male P. tridentiger dominated males of the other two species in every encounter (JV = 10 for each species pair) and P. genalutea dominated P. nigra in 16 of the 20 encounters. These differences are statistically different (P < 0.001, x 2 test). Territorial males of all three species of Petrotilapia were dominant over P. elongatus ‘aggressive’ and P. tropheops

‘orange chest’ territorial individuals in all encounters (P < 0.001, x 2 t e s t > N = 10 for each species pair). The positions of the three Petrotilapia species and the two Pseudotropheus species in a social dominance hierarchy are given in Table 3. The social ranks of the Pseudotropheus species relative to one another were obtained from Sharp (1981). The position of Petrotilapia females were derived from their relative utilizations of defended feeding sites (Table 1). It is possible that the lower two positions should be reversed based on the observations of Sharp (1981) that Petrotilapia females are frequently chased out of the territories of P. tropheops ‘orange chest’.

Table 3. Position in the social dominance hierarchy and niche breadth of three Petrotilapia sibling species and two Pseudotropheus species

Social rank Species Niche breadth

Most dominant [1] P. tridentiger territorial males 0.299 [2] P. genalutea territorial males 0.587 [3] P. nigra territorial males 0.486 [4] P. elongatus ‘aggressive’ — (individuals > 100 mm t l ) [5] P. tridentiger females 0.742 [6] P. elongatus ‘aggressive’ — (individuals < 100 mm t l ) [7] P. genalutea and P. nigra females 0.828 and 0.797 Most subordinant [8] P. tropheops ‘orange chest' — 336 A. C. MARSH AND A. J. RIBBINK.

DISCUSSION

Interspecific niche partitioning has been documented for a great variety of organisms (Schoener, 1974) and intersexual niche partitioning, although less well documented, has been shown in birds (Ward, 1965; Selander, 1966; Storer, 1966; Newton, 1967; Reynolds, 1972) and plants (Cox, 1981). In these studies it has been suggested that niche partitioning minimizes competitive interactions among and between species and consequently contributes to the maintenance of diversity. On the rocky shores at Monkey Bay epilithic algae is a limiting resource to the Mbuna (Sharp, 1981; Ribbink et al., 1983) and we believe that coexistence of the three Petrotilapia sibling species is facilitated by the interspecific and intraspecific differences in microhabitat utilization documented herein. Resource utilization in vertebrate communities is frequently dependent on an interspecific social dominance hierarchy. Dominant tend to use prime resources and to have narrower niches than subordinant animals (Morse, 1974). Furthermore, levels of aggression need not be high in such communities, as avoidance behaviour by subordinants is often well developed. In most Mbuna, including Petrotilapia, aggressiveness in males is under strong selective pressure, as only those males which can establish and maintain a territory have the opportunity to breed. Petrotilapia males are therefore preadapted to establishing dominance hierarchies. Social dominance appears to be important to the establishment and maintenance of microhabitat segregation by the Petrotilapia community. Because the amount of epilithic algae per unit area is positively correlated to the degree of defence it receives from aggressive Pseudotropheus species (Sharp, 1981), we expected the utilization of feeding sites by Petrotilapia individuals to be dependent on social rank. In general our data support this contention (Tables 1 and 3). The dominant Petrotilapia forms, territorial males, do most of their feeding in the territories of P. elongatus ‘aggressive’ and P. tropheops ‘orange chest’. The most dominant of these males, P. tridentiger, is virtually the sole user of the richest feeding sites, namely the territories of large P. elongatus ‘aggressive’ individuals. In contrast , the lowest-ranking Petrotilapia forms, females, in particular P. genalutea and P. nigra females, do most of their feeding in undefended sites. In general there is a negative correlation between dominance and niche breadth in the Petrotilapia community (Table 3). Dominant fishes are therefore more selective than subordinant fishes as to where they feed. By feeding in closely packed groups, however, subordinant Petrotilapia females can overcome the disadvantage of their low social rank and can utilize prime feeding sites (Marsh & Ribbink, in press). Feeding-site utilization is thus partly determined by the relative ease with which the various Petrotilapia forms can dominate the two aggressive Pseudotropheus species and thereby gain access to the various feeding sites. It is probably also partly mediated through acts of aggression and avoidance amongst the Petrotilapia congeners. Owing to the low frequency of aggressive encounters, it is not possible to treat this phenomenon rigorously. Anecdotal evidence, however, supports the idea that social dominance regulates feeding-site segregation. Territorial males were seen on occasion to chase congeners away from the vicinity of their feeding sites. Furthermore, P. nigra and P. genalutea territorial males and non-territorial congeners frequently move FEEDING SITES OF PETROTILAPIA 337 out of the path of approaching P. tridentiger territorial males without any overt signs of aggression from the male. Thus, we primarily attribute the coexistence of the three Petrotilapia sibling species to subtle differences in feeding behaviour which are in turn regulated by a social dominance hierarchy. Lake Malawi is renowned for the species richness of its cichlid fishes and the persistence of so many species in the lake is in part attributable to the ability of closely related species, often with very similar dietary and macrohabitat requirements, to coexist in sympatry on isolated rocky shores (Ribbink et al., 1983). We believe that further work will reveal that the coexistence of entire Mbuna communities, not just congeneric subsets as dealt with here, is due largely to two factors; so-called trophic specializations which enable fishes to utilize different food resources from the same sites, and subtle differences in the use of feeding space which are regulated by social dominance hierarchies. This latter idea supports the view that one of the keys to the success of the Cichlidae in the Great Lakes of Africa, relative to other fish families, is their elaborate behaviour (Fryer & lies, 1972).

ACKNOWLEDGEMENTS We wish to thank B. A. Marsh and A. Chunga for assisting with the field work and M. N. Bruton, B. A. Marsh, B. J. Sharp, K. R. McKaye and R. I. Yeaton for discussing aspects of this work with us. We are most grateful to the Malawi Government, Fisheries Department, for the support and hospitality extended towards us and to the South African Department of Foreign Affairs and Information for financial support.

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