Food partitioning among Lake Malawi nearshore fishes as revealed by stable isotope analyses
Harvey A. Bootsma
Within the Great Lakes of Africa there exist the world’s most diverse communities of freshwater fishes (Fryer and Iles 1972, Greenwood 1974, Ribbink et al. 1983). In particular, the nearshore waters of Lakes Malawi and Tanganyika contain flocks of species, mostly members of the family Cichlidae, which may attain densities of up to 22 species and [greater than]500 individuals in a 50-[m.sup.2] area (Ribbink et al. 1983). While many of these cichlid species are very similar in general body morphology, there is high interspecific diversity in neurocranial morphology and dentition (Fryer and Iles 1972, Reinthal 1990a). This morphological diversity suggests that interspecific differences in feeding strategies may play an important role in reducing interspecific competition and maintaining high species diversity (Fryer and Iles 1972, Reinthal 1990a). Yet the results of studies investigating feeding habits of cichlids have been equivocal. Initial studies of the stomach contents of rock-dwelling fishes (Fryer 1959, Ribbink et al. 1983) showed little or no evidence of food partitioning. This, along with laboratory studies (Liem 1984), suggested that herbivorous cichlids, while being facultative specialists, are generally nondiscriminatory feeders. In reviewing the available literature on cichlid feeding habits, Greenwood (1981:71) concluded that “there is apparently complete interspecific overlap in environmental requirement.” If this is true, then partitioning may occur only during periods of low food supply (McKaye and Marsh 1983).
More recent research (Van Oijen 1982, Reinthal 1990b) has found significant variation of stomach contents among cichlid species. However, because stomach contents represent food consumed over a small time period and within a small area, these results do not conclusively demonstrate whether food partitioning is the exception or the rule. Other disadvantages of stomach content analyses include difficulty of identification and uncertainty over whether all observed stomach contents are assimilated to the same degree, or if some components, such as cyanobacteria, are indigestible (Fryer 1959, Ribbink et al. 1983, Reinthal 1990b).
In this note we present evidence for food resource partitioning among fishes of Lake Malawi, Africa, by comparing the stable isotope composition ([[Delta].sup.13]C and [[Delta].sup.15]N) of a number of nearshore fish species and their potential food sources. Because a fish’s isotopic composition represents a spatio-temporal integration of the composition of assimilated food, this approach circumvents many of the problems in stomach analyses noted above.
Methods
Adult rock-dwelling fishes were caught in block nets at depths between 1 and 4 m at Otter Point, near the southern end of Lake Malawi. All other species were obtained by trawling in the southeast arm of the lake, except for the small cyprinid Engraulicyprus sardella (an obligate planktivore included for comparison), which was obtained from local fishermen. Except for E. sardella, which were collected in August 1992, all fish samples were collected during January and February 1991. For most fish samples only muscle tissue was analyzed, but due to their small size entire individuals of E. sardella were analyzed. A diver collected epilithic algae, sandy sediment, macrophytes, pelecypods, and gastropods by hand. Zooplankton were collected by 50-m vertical tows with a 50-[[micro]meter] mesh zooplankton net. Suspended particulate matter was collected by passing 2-3 L of water through a 50-[[micro]meter] mesh filter, to remove most zooplankton, followed by filtration onto a quartz glass fiber filter. Epilithic algae, macrophytes, sediment samples, and zooplankton were acidified before analysis to remove inorganic carbon.
Isotopic analyses were carried out on a VG Micromass 602E dual inlet mass spectrometer and a VG Optima automated mass spectrometer (VG Isotech, Middlewich, Cheshire, England) following the methods described by Hesslein et al. (1989). The instrument standard deviation is 0.05% and 0.15% for [[Delta].sup.13]C and [[Delta].sup.15]N measurements, respectively. [[Delta].sup.13]C values were determined relative to the PDB standard (the belemnite carbonate standard from the Peedee Formation, South Carolina, USA) as [[Delta].sup.13]C(%) = [([R.sub.sample]/[R.sub.standard]) – 1] x [10.sup.3], where R is the 13C:12C ratio. [Delta]15N values were determined relative to the 15N:14N ratio of air.
Results
Among the potential food sources analyzed, a strong distinction in [Delta]13C was observed between nearshore benthic samples and planktonic samples. Relative to planktonic samples, benthic samples were much more enriched in 13C and displayed a wider range of values [ILLUSTRATION FOR FIGURE 1 OMITTED]. Similar results have been reported for other aquatic ecosystems (Fry et al. 1983, Hamilton and Lewis 1992), although we are unaware of any published benthic [Delta]13C value as high as -8.1%. While small differences in [Delta]13C may result from differences in algal species composition (Zohary et al. 1994), the wide range observed in Lake Malawi is likely due to differences in the severity of C[O.sub.2] limitation (Rau et al. 1992, Hecky and Hesslein 1995) caused by large differences between pelagic and benthic photosynthetic rates (Bootsma 1993).
The [Delta]13C values measured for nearshore fishes covered a range nearly as broad as that measured for potential food sources. As expected, the semi-pelagic planktivore, Engraulicyprus sardella, had a [Delta]13C similar to that measured for zooplankton and suspended particulate carbon. Other species filled the range between planktivore and obligate benthic feeder.
While species separation was greatest along the [Delta]13C axis, [Delta]15N also proved useful in elucidating dietary differences. Several species that were poorly separated on the [Delta]13C axis were well separated on the [Delta]15N axis. For example, the difference in [Delta]13C between Oreochromis squamipinnis and Taeniolethrinops praeorbitalis is [less than]0.3%, but the [Delta]15N difference is 2.6%.
Discussion
Interpretation of isotopic composition. In comparing the isotopic compositions of different fish species and food sources, there are four factors to consider in data interpretation. (1) If two individual fishes have complete dietary overlap, they will have nearly identical isotopic compositions (DeNiro and Epstein 1978, Hesslein et al. 1991). (2) Because there is very little isotopic fractionation of carbon during trophic transfer (DeNiro and Epstein 1978, Fry and Sherr 1989), and because the increase in [Delta]15N with trophic transfer is relatively constant (between 3.0 and 5.0%, Minigawa and Wada 1984, Hesslein et al. 1991) a difference in the isotopic composition of two individuals reflects a difference in feeding strategies of those individuals. (3) If two individual fishes have similar isotopic compositions, they do not necessarily have similar feeding strategies. It is quite possible that two or more food sources have identical isotopic compositions (e.g., the macrophyte Potamogeton falls within the [Delta]13C range covered by shallow epilithic periphyton) or that a fish’s isotopic composition represents the integration of a variety of food sources with a wide range of isotopic compositions. (4) As the endpoints of the isotopic range are approached, the probability of a narrow dietary breadth increases, and relationships between food and consumers can be defined more precisely.
We observed a broad range of isotopic values among nearshore species, suggesting that these species do not feed indiscriminately (based on factor 1). Distinctions between some species, such as the lithophilous Pseudotropheus tropheops and the more pelagic Oreochromis lidole, might be expected. However, the results show that even within a monophyletic (or at least very closely related) group of “herbivores” (Fryer and Iles 1972, Ribbink et al. 1983, Moran et al. 1994; indicated with * in Fig. 1), there are large differences in feeding strategies. Pseudotropheus tropheops is an obligate periphyton feeder, while its congener, Pseudotropheus zebra, has a strong preference for plankton. For adult-fish muscle tissue, the rate at which isotopic composition responds to a change in diet is on the order of weeks to years (Hesslein et al. 1993, Peterson et el. 1993). Therefore, the observed differences in isotopic composition reflect dietary differences that persist over similar time scales or longer. Nearshore benthic photosynthesis in Lake Malawi does not appear to exhibit any seasonality that can be related to lake hydrodynamics or climatic conditions (Bootsma 1993), so it is unlikely that food partitioning prior to the sampling period was caused by lower-than-average food availability.
Among the species sampled there are several that have similar isotopic compositions. In each case there is observational evidence that these similarities result from the utilization of different food sources that have similar isotopic compositions. Within the group consisting of Protomelas taeniolatus, Ctenopharynx pictus, and Taeniolethrinops praeorbitalis [ILLUSTRATION FOR FIGURE 1 OMITTED], P. taeniolatus nips epilithic algae and benthic invertebrates, with an apparent preference for chironomid larvae (Ribbink et al. 1983), C. pictus “vacuums” rock surfaces and consumes primarily benthic copepods (Ribbink et al. 1983), and T. praeorbitalis sifts invertebrates from mouthfuls of sand (Fryer and Iles 1972). The closely grouped Petrotilapia nigra and Hemitilapia oxyrhynchus both feed on algae, but P. nigra scrapes periphyton from rock surfaces (Ribbink et al. 1983) and may feed on plankton (Reinthal 1990b) while H. oxyrhynchus nibbles periphyton off of the macrophyte Vallisneria sp, (Fryer and Iles 1972). The isotopically light [Delta]13C of Pseudotropheus zebra and Oreochromis lidole [ILLUSTRATION FOR FIGURE 1 OMITTED] indicates that both of these species rely on a phytoplankton-based food chain, but P. zebra is primarily a rock-dweller (Fryer and Iles 1972, Ribbink et al. 1983) while O. lidole lives further offshore and feeds on plankton or sandy sediment (Fryer and Iles 1972, Turner et al. 1991).
The nitrogen isotope ratio has been shown to be a useful indicator of trophic level for pelagic fishes (Fry 1988, Hesslein et al. 1991), and the general increase in [Delta]15N with size of Engraulicyprus sardella probably reflects a shift in trophic level with age. The use of [Delta]15N to infer trophic position for nearshore fishes is complicated by the possibility of differences in the [Delta]15N of the various autotrophs that form the base of near-shore food chains. At present we do not know the magnitude of these differences. However, for species belonging to food chains with the same autotroph base, the [Delta]15N will still reveal differences in trophic position. For example, Oreochromis squamipinnis and Taeniolethrinops praeorbitalis both feed on sandy sediment (Fryer and Iles 1972, Turner et al. 1991) and therefore must ultimately rely on the same autotrophic carbon source, but the difference in [Delta]15N of 2.6% between the two species suggests that O. squamipinnis is primarily an algae eater while T. praeorbitalis relies more heavily on benthic invertebrates, in agreement with the observations of this genus made by Fryer and Iles (1972). Observations of feeding habits and stomach contents (Fryer 1959, Fryer and Iles 1972, Ribbink et al. 1983) indicate that other species with high [Delta]15N values (Aulonocara sp., Protomelas taeniolatus, Ctenopharynx pictus, Trematocranus placodon) may also selectively feed on benthic invertebrates, suggesting [Delta]15N measurements will prove to be useful in accurately defining feeding strategies and trophic positions among Lake Malawi nearshore fishes.
Resource partitioning mechanisms. There are two mechanisms that may cause the distinct isotopic differences among fish species. First, species may be stenophagous, in which case the isotopic composition of a species largely reflects that of a single food source. Alternatively, species may have broad, overlapping diets, but preferences for specific food items and/or feeding locations vary between species. Among the near-shore fishes of Lake Malawi there is convincing evidence for both mechanisms. In order to be near the extremes of the [Delta]13C gradient, P. tropheops and P. zebra must be stenophagous, the former relying almost exclusively on shallow periphyton, and the latter feeding largely on planktonic organisms. This is precisely the conclusion reached by Reinthal (1990b), who found P. tropheops stomach contents to consist largely of Calothrix (a benthic filamentous cyanobacteria) while P. zebra contained abundant planktonic diatoms. Out of the seven species examined by Reinthal, these two were found to have the smallest dietary breadths.
Although some species with intermediate [Delta]13C values may also be stenophagous, the difficulty in distinguishing species based on stomach contents (McKaye and Marsh 1983, Ribbink et al, 1983, Turner et al. 1991) indicates that, for many species, there is broad dietary overlap. In this case, differences in species-specific isotopic values must be due either to spatial partitioning (i.e., a single food type may vary in isotopic composition, depending on where it is found) or to small differences in preference for specific items within the food suite. In fact, selection for specific food resources may often be achieved by spatial partitioning, since the ability of most species to selectively pick out specific food items from a given micro-habitat is probably very limited (Ribbink et el. 1983). For some of the species analyzed, there already exists evidence of spatial partitioning. Among the Oreochromis species, adult O. lidole are considered the most pelagic (Fryer and Iles 1972, Turner et al. 1991), and the [Delta]13C data support this belief.
Interspecific differences in isotopic composition, combined with similarity in stomach contents, imply that species using similar food types occupy different habitats. Conversely, in order to have different isotopic compositions, species occupying the same habitat must utilize different food types. Such a lack of interspecific correlation between the use of two resources (food and space), which Schoener (1974) calls “complementarity,” is a strong indication that feeding differences are not the result of stochastic variability, but are the product of competition and specialization. The data presented here provide preliminary evidence that such complementarity exists among nearshore fishes in Lake Malawi.
Acknowledgments: We are grateful to the Malawi Department of National Parks and Wildlife and the Malawi Fisheries Department for permission to conduct research in Lake Malawi. We also thank P. Ramlal for carrying out stable isotope analyses. G. Patterson provided some of the plankton and pelagic fish samples. Financial support was provided by an IDRC Young Canadian Researchers Award to H.A. Bootsma, an NSERC research grant to R.E. Hecky, and the Department of Fisheries and Oceans Canada. E. Fee, D.W. Schindler, G. Mittelbach, and three anonymous reviewers provided useful comments on early drafts of the manuscript.
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