Sep 26, 1991 - The Aufwuchs-eating cichlids of Lake Tanganyika show clear trophic differences that are correlated to their morphology, physiology and ...
Environmental 0 1992 Kluwer
Biology of Fishes 35: 283-290, Acade,mic Publishers. Printed
1992. in the Netherlands.
Ecophysiology of Aufwuchs-eating cichlids in Lake Tanganyika: niche separation by trophic specialization Christian Sturmbauer*,
Wolfgang Mark & Reinhard Dallinger
Institute of Zoology, Department of Zoophysiology, Universi& of Innsbruck, Technikerstr. 25, A -6020 Znsbruck Austria * Present address: Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY 11794-5245, U.S.A. Received
27.11.1990
Accepted
26.9.1991
Key words: Feeding, Diet, Nutrition,
Intestinal length, Digestive enzymes, Trypsin, Amylase, Laminarinase
Synopsis The Aufwuchs-eating cichlids of Lake Tanganyika show clear trophic differences that are correlated to their morphology, physiology and foraging behaviour. The species are grouped into three categories of relative intestinal length according to their feeding habits. A correlation between the intestinal length and the diet could be demonstrated, ranging from around 2.5 for species ingesting more animal food, to 7.8 for detritivorous and microalgivorous species. The relative intestinal length of domestic Tropheus moorii, raised in aquaria was significantly lower than that of wild individuals by a factor of 1.7, demonstrating a wide range of phenotypic adaptability. The activities of trypsin and amylase were at an equal level in four Aufwuchseating species, but the activity of laminarinase of a detritivorous-microalgivorous species (Petrochromis orthognathus) was 2.6 times higher than that of an algivorous species (Tropheus moorii). The laminarinase seems to be an excellent marker enzyme for detritivorous or microalgivorous feeding.
Introduction Lake Taganyika presents one of the most peculiar tropical freshwater ecosystems. Specific chemical parameters isolate the lake from surrounding waters; this has led to the evolution of an endemic fish fauna, dominated by cichlid species. By adaptive radiation these species have colonized different habitats of the lake. The species community of rocky coasts is based on Aufwuchs, a thin biocover of algae, microorganisms, sponges, small crustaceans and detritus. About 20 cichlid species are considered to be Aufwuchs-eaters (Yamaoka 1983). These sympatric species are able to coexist on account of their slightly different feeding habits and diets. The present study compares the feeding
habits of four sympatric species with respect to morphological and physiological parameters. The activities of three digestive enzymes are reported: amylase, trypsin and laminarinase.
Material and methods The investigation was carried out in March 1985 and in February and March 1988 in Magara (3”44’ South, 29”19’ East), 41 km South of Bujumbura, Republic of Burundi. Four sympatric species with different feeding habits were selected: Tropheus moorii, Simochromis diagramma, Petrochromis orthognathus and Eretmodus cyanostictus. Fish
were collected at depths between 0.7 and 1.5 me-
284
ters. In order to obtain fish with full stomachs and intestines, they were collected in the early afternoon using a hand- or gill-net and dissected within 30 minutes. Stomach and intestine were carefully unfolded and their lengths measured. The relative intestinal length (RIL = intestinal length/standard length) and the intestinal weight lengths (IWL = intestinal length [cm]pv volume [ml]) were calculated according to Zihler (1982). Diet analysis. The intestinal content was analyzed
microscopically according to the points method (Hynes 1950). This method was chosen in order to provide comparability to previous detailed works from Takamura (1984), Yamaoka et al. (1986) and Mbomba (1986). All samples were taken at the same season. The stomach and the anterior part of the intestine were fixed in 4% formalin solution. From each individual, 5% of the total content were sampled in multiple aliquots. The total content of each aliquot was analyzed. The size of sand particles was determined by means of an ocular micrometer. Their size turned out to be highly uniform, hence the volume of the most frequent size class of sand particles was defined as 1 volume-unit. The volumes of all occuring items were related to this unit. Due to the highly variable size of detritus its volume was estimated in multiple monolayers relative to all other components. The single estimations were averaged for each individual. Diatoms were too small to be counted in terms of volume and only relative frequences were estimated (+/ ++/+ ++). Dietary items were not weighed according to their nutritive value by the inclusion of the ‘importance factor’ (Hynes 1950). In Tropheus moorii the diets of juveniles (SL = 40-50 mm) and adults (SL = 77-105 mm) were analyzed separately in order to determine eventual differences (Table 2). The last fifth of the gut, resembling the colon, was discarded. The remainder was divided into three sections, the contents of which were collected separately. The contents of the intestinal sections of Eretmodus cyanostictus were pooled for the determination of pHvalue and enzyme activities. After centrifugation, Preparation of intestinalfluids.
small aliquots (3 to 10~1) of the intestinal fluid were preserved for future analysis. The intestinal fluids of Eretmodus cyanostictus were precipitated with ethanol (one part intestinal fluid to two parts 96% ethanol) and dried in a desiccator. In the intestinal fluids of Tropheus moorii and Petrochromis orthognathus, recovery was incomplete, probably due to interfering plant proteins. Therefore, ethanol precipitation was avoided and small portions of the supernatant were dried in a desiccator. The samples were stored in a refrigerator until estimation of the enzyme activity. The stability of trypsin and amylase after precipitation in ethanol and/or drying was extensively tested (Hofer & Kock 1989, Kock & Hofer 1989). In measurements using the intestinal fluids of Oreochromis leucostictus, equal enzyme activities were recovered after precipitation and drying the intestinal fluid. Determination of amylase and trypsin activities. In the laboratory the dried supernatants of the intestinal fluids were rediluted in triethanolamineHCl buffer (pH 7.5, 1% NaCl, 0.3% CaCl,). After thorough mixing, the activity of amylase was determined photometrically (405 nm) using the amylase test of Boehringer Mannheim. The tryptic activities were measured photometrically (248 nm) using TAME (p-tosyl-L-argininemethylester . HCl, 10 mM, pH = 8.5) as substrate (Bergmeyer 1974). The mean activities were compared using Student’s t-test. of laminarinase activity. The laminarinases hydrolyse (l-3); (l-6)P-D-glucans, such as laminarine, the main polysaccharide in Phaeophyta, and chrysolaminarine, the main polysaccharide of diatoms. The laminarinase activity had to be determined in the field, because the enzyme appeared to be irreversibly destroyed by freezing and ethanol precipitation. Aliquots of intestinal fluids were mixed with equal amounts of a buffered substrate solution (Laminarine Sigma L 9634, 10 mg ml-‘, pH 5.0), and incubated at 25” C in a time series, following the digestion of laminarine to glucose. A control with buffer solution was also included. The digestive process was stopped by precipitating the incubation mixture with ethanol (one Determination
285 part incubation mixture to two parts 96% ethanol). The precipitation irreversibly denaturated the enzyme and conserved the metabolites for future analysis. Samples were stored in a refrigerator and analyzed by means of a HPLC-Column specific for carbohydrates (Bio Rad HPX 87H). The activities of laminarinase were based on the time required for hydrolysis of half of the substrate (1 Unit = 1 pug glucose produced per minute).
Food analysis. The present analysis differs from all former ones in that high amounts of detritus were found to have been ingested by all of the species studied (Table 1). 7: moorii selectively fed on filamentous epilithic algae (35%), but also ingested 38% detritus and 25% sand covering the epilithic algae. The dominating species among filamentous algae was ClaSmall portions of diadophora sp. (Chlorophyta). toms and other microalgae were also identified. Detritus (58%) and sand (35%) were the dominant constituents of the diet of P. orthognathus.
High numbers of diatoms, mainly Pennales and (Pediastrum sp.) were unicellular Chlorophyta identified; in contrast to T moorii, filamentous algae accounted for only 1% of the total volume. Petrochromis orthognathus is considered to be a detritus- and microalgae-comber which occasionally also may catch prey. The diet of Eretmodus cyanostictus also mainly consisted of detritus (35%), but sand made up only 12.5%. Apart from 26% of filamentous algae, animal food items accounted for 16% of the total volume. It is concluded that this species is more selective in catching prey. Relative intestinal length (RIL) and Intestinal weight length (IWL). Petrochromis orthognathus, a
detritivorous and microalgivorous species, had significantly higher IL and IWL (6.4; 19.1) than Tropheus moorii (4.8; 14.1; p < 0.0001) and Simochromis diugramma (4.0; 12.2; p < 0.05), both feeding selectively on filamentous algae. Eretmodus cyanostictus, ingesting the highest percentage of animal food, had the shortest intestine (2.46; 7.8; p < 0.0001; Table 2). Furthermore, the relative intestinal lengths of
Table 1. Food-analysis of three Aufwuchs-eating species of Lake Tanganyika. Diet categories are quantified in % of total volume according to the points method (Hynes 1950). The following categories were defined: Detritus = sedimenting organic matter, forming a sp.); diaroms and other unice/lular thin layer over the epilithic algae. Filamentous algae = chlorophyta (dominated by Cladophora algae = Chrysophyta (Diatomaeae, mainly Pennales); Chlorophyra (Pediastrum sp.); Cyanophyta (Gloeotrichia sp.). Items of this category were identified but were too few to be quantified in terms of volume. Crustaceans = ostracods, copepodes and cladocerans.
Fond items Detritus Filamentous algae Macrophyte tissue Diatoms Total
38.2 35.0 + 35.0 1.4
plants
Crustaceans Rotifers Insects Chironomid larvae Invertebrate eggs Unidentified animals Total
Tropheus
animals
Sand Number of individuals Total points
moorii
Petrochromis
58.2 1.0 I.0 + + -t 2.0 1.0
2.4 -
1.4 25.4
11 1100
orthognarus
Eretmodus
35.4 26.0 10.1 +
-
36.1 2.7 0.1 12.1 0.2
3.4 35.4
4 824
0.9 16.0 12.5
10 1172
cyanostictus
286 three adult Tropheus moorii raised in captivity were determined. Due to the higher nutritive value and low fibre content of the flake food the RIL of captive Tropheus moorii was shorter than that of wild animals by a factor of 1.7 (p< 0.0001; see Table 2).
found in Petrochromis orthognathus (p< 0.05). This correlates with the different feeding habits (Table 3).
Amylase and trypsin. The activities of amylase and trypsin were similar in all species measured. Petrochromis orthognathus had the highest (378 U ml’) and Simochromis diagramma the lowest (304 U ml-‘) amylase activities. Simochromis diagramma
The cichlid fishes of Lake Tanganyika went through a unique adaptive radiation, during which they colonized numerous ecological niches (Fryer & Iles 1972, further references in Echelle & Kornfield 1984). Liem (1973) introduced the idea that the special design of the trophic apparatus in combination with a broad repertoire of feeding behaviour was the key to this successful radiation. He hypothesized that the rapid evolution of this group is due to the high adaptive efficiency of morphological changes, i.e. even slight morphological variations allow the fish to exploit new source of food (Liem & Osse 1975; Liem 1980, 1984). However, evidence of a high degree of phenotypic plasticity and trophic polymorphism in cichlids, is accumu-
Discussion
had the highest tryptic activity (221 U ml-‘; p < 0.02), that of Tropheus moorii amounted to 163 U ml-‘, Eretmodus cyanostictus and Petrochromis orthognathus had the lowest activities (157 U ml-‘). The activities decreased considerably in the posterior sections of the intestine (Table 3). Laminarinase. In contrast to the former enzymes there is a 2.6-fold difference between the activities of laminarinase in Tropheus moorii and those
Table2. Relative intestinal length (RIL) and intestinal weight length (IWL) of four Aufwuchs-eaters with different feeding habits from Lake Tanganyika. Means and standard deviations (in brackets) are given. Abbreviations: SL = standard length; n = number of individuals; n.d. = not determined. * Calculation of ‘intestinal weight length’ (Zihler 1982): IWL = intestinal length (cm)/)V Volume (ml).
Species
RIL
IwL*
major constituents of the diet
Petrochromis orthognathus
6.4 (0.3) n= 4
19.1 (1.4) n= 4
Tropheus moorii,
4.8 (0.5) n= 24
14.1 (1.6) n= 22
Tropheus moorii,
4.0 (0.4) n= 3
10.5 (0.6) n= 2
Simochromis diagramma
4.0 (0.6) n= 2
12.2 (2.2) n= 2
58% detritus, 35% sand, 3% animals 38% detritus, 35% filamentous 25% sand 38% detritus 35% filamentous 25% sand 63% filamentous 8% sand, 6% macrophyte kamura (1984) 35% detritus, 26% filamentous 16% animals
SL: SO-90mm adult SL: 77-105 mm juvenile SL: 40-50 mm
SL: 6&70mm Eretmodus cyanostictus
2.46 (0.5) n= 30
7.8 (1.5) n= 30
2.8 (0.1) n= 3
n.d.
SL: 33-68mm T moorii
adult SL: 85-90mm
algae,
algae, algae, tissue, analysis of Ta-
algae,
mainly flake food (raised in captivity)
287 lating (ref. in Meyer 1990a). Greenwood (1965) first noticed extensive intraspecific morphological variability of the pharyngeal jaw apparatus (PJA). The morphology of the trophic apparatus depends on the ontogenetic feeding history, as demonstrated for the African cichlid Haplochromis squamipinnis (Witte 1984) and for the neotropical Cichlasoma species (Meyer 1987). Polymorphisms were also found in African and neotropical cichlids (Greenwood 1959, Hoogerhoud 1986, Kornfield & Taylor 1983, Meyer 1990a, 1990b). Not only the trophic apparatus, but also the intestine is adapted to different ecological conditions at the level of morphology and physiology; Hofer (1988) demonstrated different styles by which the intestinal mucosa of cyprinids and of a cichlid are increased in response to diets of low digestibility or inferior nutritional value. The constant feedback between diet and intestinal morphology is supported by our finding of a striking difference in the intestinal length between domestic and wild Tropheus moorii. On the physiological level, the activities of digestive enzymes are triggered by the composition of the diet (Kawai & Ikeda 1972, Hofer 1979a, 1979b, Niederholzer & Hofer 1979, Sturmbauer & Hofer 1986). Many morphological structures and physiological parameters can change rapidly according to environmental factors, so that they cannot be considered characteristics of a species without being studied in relation to the immediate environmental conditions. Laboratory exTable 3. Activities of trypsin, amylase and laminarinase of the anterior intestine in Aufwuchs-eating cichhds of Lake Tanganyika. Means and standard deviations (in brackets) are given. Abbreviations: n.d. = not determined, n = number of samples, * = intestinal fluid of several individuals pooled, I Activity: 1U ml-’ = 1 pg glucose turnover per minute per ml intestinal fluid.
Species
Trypsin
Amylase
Laminarinase’
T moorii
163~(19) 11 15g (40) n= 3 157 (25) n= 5* 221 (32) n= 4
311 n= 378 n= 332 n= 304 n=
133 (66) n= 3 352 (127) n= 4 n.d.
n=
P. orthognathus E. cyanostictus S. diagramma
(175) 11 (188) 3 (51) 5* (34) 4
n.d.
periments can determine the range of adaptive flexibility (reaction norm), but one has to be aware that it is the specific environment that modifies the expression of the phenotype. The PJA of Astatoreochromis alluaudi not only varied according to the abundance of snails in the lakes the species occured, but also depended on the presence of other haplochromines. In some lakes, where Astatoreochromis alluaudi had been introduced and competition was absent, it lost its hypertrophic pharyngeal teeth and preferred ‘soft’ invertebrates instead of snails (Witte et al. 1990, Witte personal communication). Competition for food between the members of a community may play a dominant role in forcing a species into a particular niche. The partitioning of resources by trophic specialization seems to be one driving force of speciation. The present study tested different biological parameters connected to nutrition in order to distinguish the niches of Aufwuchs-eaters of Lake Tanganyika. The relative intestinal length (RIL) is an easily measured criterion for intestinal specialization to different feeding regimes (Hofer & Schiemer 1981, Ribble & Smith 1983). We group the Tanganyikan Aufwuchs-eaters into three classes based on intestinal length. The detritivorous and microalgivorous species, e.g. Petrochromis orthognathus, have the longest intestines (RIL 6-10). Feeders of filamentous algae form a second class, with an RIL between 4 and 5, e.g. Tropheus moorii and Simochromis diagramma. The higher proportion of animal food items found in Eretmodus cyanostictus is associated with shorter intestines (RIL 2.5-3.0). Spathodus erythrodon, Tanganicodus irsacae and Lobochilotes labiatus have comparable dietary compositions and RIL between 2.0 and 2.5 (Yamaoka et al. 1986). In two species, not considered Aufwuchs-eaters, Lepidolamprolous elongatus and Lamprichthys tanganicunus (Cyprinodontidae), the RIL were below 1. The present analysis shows remarkable parallels to Aufwuchs-eating cichlids of Lake Malawi (Reinthall990). In Lake Malawi, species could be differentiated by characteristic relative frequences of food items, despite of a high degree of overlap. As many species were sampled at greater depths, diatoms were more abundant food items in those spe-
288
ties. Our study differs from previous ones by the inclusion of detritus in the analysis. We found high amounts of detritus in all Aufwuchs-eating species, regardless of their dietary preferences. Epilithic algae are covered by a layer of detritus that is permanently renewed by wave action. Consequently, detritus is forcibly ingested along with the preferred diet. However, a number of species specialized on detritivorous feeding by high consumption rates along with extremely elongated intestines. Behavioural observations on Tropheus moorii demonstrated that feeding was by far the most frequent behaviour (Sturmbauer 1990, Sturmbauer & Dallinger unpublished). The comparison of the activities of the digestive enzymes trypsin and amylase did not reveal significant differences between four Aufwuchs-eating species. The well established correlation between protein or starch content and the enzyme activities, could not be confirmed in the trophic group of Aufwuchs-eaters (Nagase 1964, Kawai & Ikeda 1972, Hofer & Schiemer 1981). Only in Simochromis diagramma was a significantly higher tryptic activity found (p < 0.02). Another digestive enzyme, laminarinase, seems to be an excellent marker for specialized detritivorous or microalgivorous feeding. The laminarinase activity of Petrochromis orthognathus significantly exceeded that of Tropheus moorii by a factor of 2.6 (p < 0.05). All species of the genus Petrochromis use their tricuspid teeth to comb detritus and diatoms from the substrate (Mbomba 1983, 1986, Yamaoka 1982, 1983,1988). In contrast, members of the genera Tropheus, Simochromis and Pseudosimochromis have dicuspid teeth to bite off mainly filamentous algae from the substrate and also ingest some adhesive detritus and unicellular algae. Laminarine-like carbohydrates are found in diatoms (Chrysophyta), some microorganisms, but not in Chlorophyta or Cyanophyta. Therefore, microalgivorous and/or detritivorous species should have higher laminarinase activities. In vertebrates, only phytophagous freshwater teleosts have an endogenous laminarinase (Piavaux 1972, Piavaux 1977). Feeding experiments with a semisynthetic diet containing pure laminarine (Sigma L9634)
showed that only cichlids are able to digest laminarine completely by means of the debranching enzyme, which is lacking in cyprinids (Sturmbauer 1990, 1991). Piavaux & Dandrifosse (1972) measured the laminarinase activity of different tissues of Tilapia macrochir. They found high activities in the anterior intestinal mucosa, which releases the enzyme into the lumen. The analysis of the in-vitrodigests by means of HPLC proved that the enzymes of teleosts act as exoenzymes (Sturmbauer 1990, 1991). As most of the microorganisms have only endolaminarinases, the observed activity conceivably originates from the fish itself. In Lake Tanganyika complex interspecies interactions evolved between members of the community of Aufwuchs-eaters (Mbomba 1986). Correlations between interspecies aggression and similarity of diet were recorded (Takamura 1984) and symbiotic relationships between sympatric Aufwuchs-eaters were found (Takamura 1983, Sturmbauer unpublished). McKaye & Marsh (1983) hypothesize that morphological specializations become more critical in times of food scarcity. In periods of abundance, two algae-scraping cichlids from Lake Malawi fed facultatively. The survival of such bottleneck periods by an effective niche separation is a prerequisite for the formation of stable species communities. Other authors consider Aufwuchs as a limited source of food for most of the year (Reinthal 1990). Our dietary analyses also show an overlap of diet. Some items, like detritus, are forcibly ingested along with the preferred diet. Rare or elusive prey items are ingested opportunistically by all Aufwuchs-eaters; they are not considered frequent diet items. Nevertheless, all observed species showed clear frequency differences in their diet that were correlated to their morphology, physiology and foraging behaviour. At present, very little information about local and seasonal differences of dietary composition is available, and more data are needed. However, there is increasing evidence that most cichlids exhibit enormous behavioural, morphological and physiological flexibility in spite to their remarkably high degree of morphological specialization. In our opinion this flexibility is the key to explaining the
289 explosive radiations, in which adaptive differentiations are morphologically manifested during the process of speciation.
Acknowledgements We thank Joy and Wolfgang Wieser, Rudolf Hofer and Axe1 Mayer for reviewing the manuscript. We should also like to thank Harry Johnson, Bujumbura, for his hospitality and M. Boniface Nyakageni, Ministry of Water and Forests, Republic of Burundi, for the research permission.
References cited Bergmeyer, H.U. (ed.) 1974. Methods in enzymatic analysis. Verlag Chemie, Weinheim. Vol. 1, pp. 1060-1062. Echelle, A.A. & I. Kornfield (ed.) 1984. Evolution of fish species flocks. University of Maine Press, Orono. 257 pp. Fryer, G. & T.D. Iles. 1972. The cichlid fishes of the great lakes of Africa. Oliver & Boyd, Edinburgh. 641 pp. Greenwood, P.H. 1959. The monotypic genera of cichlid fishes in Lake Victoria, Part II. Bull. Brit. Mus. Nat. Hist. (Zoo].) 5: 165-177. Greenwood, P.H. 1965. Environmental effects on the pharyngeal mill of a cichlid fish, Astatoreochromis alluaudi and their taxonomic implications. Proc. Linn. Sot. London 176: l-10. Hofer, R. 1979a. The adaption of digestive enzymes to temperature, season and diet in roach Rutilus rutilus L. and rudd Scardinius erythrophthalmus L. - Amylase. J. Fish Biol. 14: 565-572. Hofer, R. 1979b. The iadaption of digestive enzymes to temperature, season and diet in roach Rutilus rutilus L. and rudd Scardinius erythrophthalmus L. - Proteases. J. Fish Biol. 15: 373-379. Hofer, R. 1988. Morphological adaptations of the digestive tract of tropical cyprinids and cichlids to diet. J. Fish Biol. 33: 399-408. Hofer, R. & G. K&k. 1989. Method for qualitative determination of digestive enzymes in fish larvae. Pol. Arch. Hydrobiol. 36: 439-441. Hofer, R. & F. Schiemer. 1981. Proteolytic activity in the digestive tract of several species of fish with different feeding habits. Oecologia 48: 342-345. Hoogerhoud, R.J.C. 1986. Taxonomic and ecological aspects of morphological plasticity in molluscivorous haplochromines (Pisces, Cichlidae). Ann. Mus. Roy. Afr. Centr. SC. Zoo]. 251: 131-134. Hynes, H.B.N. 1950. The food of freshwater sticklebacks (Gas-
terosteus aculeatus and Pygosteuspungitius), with a review of methods used in studies of the food of fishes. J. Animal Ecol. 19: 36-58. Kawai, S. & S. Ikeda. 1972. Studies on the digestive enzymes of fishes - II. Effect of dietary changes on the activities of digestive enzymes in carp intestine. Bull. Jap. Sot. Sci. Fish 38: 265-270. K&k, G. & R. Hofer. 1989. The effect of natural and artificial diets upon tryptic activity of roach (Rutilus rutilus) and whitefish (Coregonus sp.) larvae. Pol. Arch. Hydrobiol. 36: 443453. Kornfield, I. & J.N. Taylor. 1983. Anew speciesof polymorphic fish, Cichlasoma minckleyi, from Cuatro Cienegas, Mexico (Teleostei: Cichlidae). Proc. Biol. Sot. Wash. 92: 253-269. Liem, K.F. 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst. Zool. 22: 425-441. Liem, K.F. 1980. Adaptive significance of intra- and interspecific differences in the feeding repertoire of cichlid fishes. Amer. Zoo1 20: 295-314. Liem, K.F. 1984. Functional versatility, speciation and niche overlap: are fishes different? pp. 269-305. In: D.G. Meyers & J.R. Strickler (ed.) Trophic Interactions Within Aquatic Ecosystems, AAAS Selected Symposium 1985. Liem, K.F. & J.W. Osse. 1975. Biological verstility, evolution and food resource exploitation in African cichlids. Amer. Zool. 15: 427-454. Mbomba, N.B. 1983. Comparative morphology of the feeding apparatus in cichlidian algal feeders of Lake Tanganyika. Afr. Stud. Monogr. 3: l-23. Mbomba, N.B. 1986. Comparative feeding ecology of Aufwuchs eating cichlid fishes in Lake Tanganyika with reference to their developmental changes. Physiol. Ecol. Japan 23: 79-108. McKaye, K.R. & A. Marsh. 1983. Food switching by two specialized algae-scraping cichlid fishes in Lake Malawi, Africa. Oecologia 56: 245-248. Meyer, A. 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357-1369. Meyer, A. 1990a. Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol. J. Linn. Sot. 39: 279299. Meyer, A. 1990b. Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. J. Zool. Lond. 221: 237-260. Nagase, G. 1964. Contribution to the physiology of digestion in Tilapia mossambica Peters: digestive enzymes and the effects of diet on their activity. Z. vergl. Physiol. 49: 270-284. Niederholzer, R. & R. Hofer. 1979. The adaption of digestive enzymes to temperature, season and diet in roach Rutilus rutilus L. and rudd Scardinius erythrophthalmus L. - Cellulase. J. Fish Biol. 15: 411-416. Piavaux, A. 1972. Intestinal laminarinase of a vertebrate: Tila-
290 macrochir Boulenger (Teleostei, Cichlidae). Life Sciences 11: 185-190. Piavaux, A. 1977. Distribution and localization of the digestive laminarinases in animals. Biochem. System. Ecol. 5: 231-239. Piavaux, A. & G. Dandrifosse. 1972. Presence de laminarinases dans I’intestin d’un Poisson cichlidae Tilupiu macrochir Boulenger. Arch. Int. Physiol. Biochim. 80: 51-57. Reinthal, P.N. 1990. The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi, Africa. Env. Biol. Fish. 27: 215-233. Ribble, D.O. & M.H. Smith. 1983. Relative intesine length and feeding ecology of freshwater fishes. Growth 47: 292-300. Sturmbauer, C. 1990. Vergleichende Untersuchungen zur Physiologie und Ethologie herbivorer Fische. Thesis, University of Innsbruck, Innsbruck. 130 pp. Sturmbauer, C. 1991. Different enzymes for laminarine digestion in Chondrostoma nasus (Cyprinidae) and Oreochromis sp. (Cichlidae). Comp. Biochem. Physiol. BlOO: 199-202. Sturmbauer, C. & R. Hofer. 1986. Compensation for anylase inhibitors in the intestine of the carp (Cyprinus curpio). Aquaculture 52: 31-33. Takamura, K. 1983. Interspecific relationship between two Aufwuchs-eaters Petrochromispolyodon and Tropheus moorii (Pisces, Cichlidae) of Lake Tanganyika, with a discussion on the evolution and functions of a synbiotic relationship. Physiol. Ecol. Japan 20: 5969. piu
Takamura, K. 1984. Interspecific relationships of Aufwuchseating fishes in Lake Tanganyika. Env. Biol. Fish. 10: 225241. Witte, F. 1984. Consistency and functional significance of morphological differences between wild-caught and domestic Huplochromis squumipinnis (Pisces: Cichlidae). Netherl. J. Zool. 34: 596612. Witte, F., C.D.N. Bare1 & R.J.C. Hoogerhoud. 1990. Phenotypic plasticity of anatomical structures and its ecomorphological significance. Nether]. J. Zool. 40: 278-298. Yamaoka, K. 1982. Morphology and feeding behaviour of five species of genus Petrochromis (Teleostei, Cichlidae). Physiol. Ecol. Jap. 19: 57-75. Yamaoka, K. 1983. Feeding behaviour and dental morphology of algae scraping cichlids (Pisces: Teleostei) in lake Tanganyika. Afr. Stud. Monogr. 4: 77-89. Yamaoka, K. 1988. Comparative osteology of the suspensoral complex of algal-feeding cichlids (Pisces, Teleostei) from Lake Tanganyika. Afr. Stud. Monogr. 9: 65-84. Yamaoka, K., M. Hori & S. Kuratani. 1986. Ecomorphology of feeding in ‘goby-like’ cichlid fishes in Lake Tanganyika. Physiol. Ecol. Jap. 23: 17-29. Zihler, F. 1982. Gross morphology and configuration of digestive tracts of cichlidae (Teleostei, Perciformes): phylogenetic and functional significance. Nether]. J. Zool. 32: 544-571.
