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Ecomorphological Diversification and Convergence in Fluvial Cichlid Fishes

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Ecomorphological Diversification and Convergence in Fluvial Cichlid Fishes Environmental Biology of Fishes 44: 235-261, 1995. @ 1995 Kluwer Academic Publishers. Printed in the Netherlands. Ecomorphological diversification and convergencein fluvial cichlid fishes Kirk O. Winemiller,! Leslie C. Kelso-Winemiller! & Antoinette L. Brenkerf J Department of Wildlife and FisheriesSciences, Texas A&M University, CollegeStation, TX 77843-2258,US.A. 2 Environmental SciencesDivision, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6036,US.A. Received 15.12.1993 Accepted 24.10.1994 Key words: Adaptive radiation, Convergent evolution, Costa Rica, Diet, Phylogeny, Venezuela, Zambia Synopsis We compared ecological and morphological patterns among cichlid faunasfrom three different biotic regions: the Rio Tortuguero/Rio Sarapiqui in Costa Rica, the Rio Apure drainage in Venezuela, and the Upper Zam- bezi drainage in Zambia. Cichlids comprise 19percent of the fish fauna in the Tortuguero and Upper Zambezi drainagesand 6.5 percent in the Apure drainage. Cichlid faunas exhibited similar patterns of habitat and food resource utilization, although vegetation-dwelling is more common and detritivory and herbivory are rarer in the Apure fauna. We hypothesize that South American ostariophysan fishes were more pre adapted than cichlids to exploit detritivore and herbivore niches. The Zambezi cichlid fauna showsless ecomorphological diversification than the other two faunas, even though the degree of dietary diversification is similar among faunas. Chaetobranchusflavescens from the Venezuelanfauna is the only speciesthat specializeson zooplank- ton as an adult, and algae grazing (Neetroplus nematopus) and specialized fruit feeding ('Cichlasoma' tuba) were represented only in the Costa Rican fauna. Based on the most recent hypothesized phylogeny for the family Cichlidae, we identified numerous interfaunal ecomorphological and feeding niche convergences.Pat- terns of ecomorphological divergence in relation to cladogenesisindicate a faster rate of evolutionary niche diversification in Central American cichlids compared with the two other faunas. Introduction functional versatility in the feeding apparatus among species of haplochromine cichlids of the Ecomorphology is the field of study that examines African rift lake speciesflocks. In nearly all cases relationships between functional morphology and examined, versatility in motor patterns permitted ecological performance. Functional morphology is both specialized feeding modes as well as general- usually studied under controlled conditions in the ized feeding on a fairly wide variety of prey in the laboratory (Alexander 1970, Liem 1980, Lauder laboratory. Liem (1991)questioned whether or not 1983),however it can be pursued in the field setting morphological specializationsin these diverse fish- (Yamaoka ~982).In contrast and by definition, ec- es necessarilytranslated into ecological segregation ological studies require the investigation of orga- in the field setting. Several studies have shown vari- nisms in a field setting. Developments at the theo- able diets within populations of African lake-dwell- retical interface between functional morphology ing cichlids (McKaye & Marsh 1983,Ribbink et al. and ecology have been, to some extent, hindered by 1983,Witte 1984).Other studies have documented weak linkages between laboratory and field data. specializations in the foraging behaviors and diets For example, Liem & Osse (1975) demonstrated of individual fishes within populations of Lake Tan- 236 ganyika haplochromines (Yamaoka 1982, 1983, tion in the tungara frog (Physalaemus)provides an 1991,Hori 1983). To date, few field studies have illuminating example (Ryan 1985,Rand et al.1992). achieved sufficient detail to demonstrate the associ- Motta & Kotrschal (1992)also listed several pitfalls ation between the frequency of utilization of alter- in ecomorphology, including: (1) selection of inap- native feeding modes, resource utilization, and in- propriate characters for the question, (2) selection terspecific niche segregationwithin fish assemblag- of an inappropriate analysis, (3) lack of a null hy- es. pothesis, (4) lack of knowledge of life history, and Imperfect knowledge of phylogenetic relation- (5) lack of knowledge of constraints, both genetic ships poses an additional problem for advancesin and morphological. ecomorphology. Even if ecological specializations Sparked by Hutchinson's (1959) seminal paper, can be demonstrated in the field, closely related ecologists haye invoked the theory of ecomorphol- speciesmight be expected to exhibit similar feeding ogy in studies of community organization (MacAr- behaviors and diets due to inherited phenotypic thur & Levins 1967, Fenton 1972, Hespenheide similarities. Adaptive radiations in form, function, 1973,Karr & James1975). Gatz (1979a,1979b, 1981) and ecology provide evidence of ecomorphological was among the first to examine the covariance relationships, however interpretations even of the among morphological traits of known function in same data can sometimes vary. For example, Liem fish assemblages,and the covarianceof morpholog- (1991)and Yamaoka (1991)differed in their inter- ical traits with ecological traits. Severalstudies have pretations of morphological and ecological diversi- followed Gatz's paradigm to explore additional as- fication in African rift lake cichlids as evidence for pects of fish community organization (Felley 1984, adaptive radiation. The demonstration of conver- Moyle & Senanayake1984, Page & Swofford 1984, gent morphological traits and associatedecological Watson & Balon 1984, Grossman 1986, Douglas performance is perhaps our most powerful means 1987,Strauss 1987, Wikramanayake 1990,Winemill- of documenting ecomorphological relationships er 1991a).The successof this community paradigm (Orians & Paine 1983, Motta & Kotrschal 1992). has resulted in frequent interpretations of patterns Studies of convergent evolution require robust hy- of covariation among morphological traits with pothesesof phylogenetic relationship, and the lack known functions in the context of ecological inter- of a high degree of phylogenetic resolution in large actions. Following this approach,ecomorphological cladeshas retarded this area of inq uiry (Winemiller theory is effectively substituted for the absenceof 1991a,1992). Meyer et al.'s (1990) molecular study mechanistic evidence from field studies (e.g., Wer- of phylogenetic relationships and parallelism ner 1977). among African rift lake cichlids illustrates how The present study integrates elements 1 and 5 of well-resolved phylogenetic data facilitate robust in- Motta & Kotrschal's (1992) research paradigm to terpretations of morphological diversification. reveal patterns of ecomorphological divergence Motta & Kotrschal (1992) recently outlined the and convergence among species assemblages.We steps for a research program in ecomorphology. examine patterns of morphological and ecological They proposed that initial steps should involve: (1) diversification and convergence in river-dwelling the study of the relationships (covariance) between cichlids from three biotic regions: south-central environmental factors and form, (2) performance Africa, northern South America, and Central testing, (3) examination of optimization and con- America. Morphological traits were selectedbased straints on form-function relationships, (4) investi- on assumptions of optimal performance and func- gation of the ontogeny of form-function relation- tional constraints (Motta & Kotrschal's elements ships,and (5) examination of the direction of evolu- 2-3) from earlier functional morphology (e.g., tion in form-function relationships. Rarely are all Alexander 1970,Lauder 1983) and ecomorpholog- five elements incorporated into ecomorphological ical studies of fishes (e.g., Gatz 1979a,Webb 1984). research,although Ryan and Rand's studies of pre- We adopt Winemiller's (1991a)approach for com- dation, sexual selection, and evolution of vocaliza- paring faunas and examining hypotheses of eco- 237 morphological convergence and divergence. The Regional cichlid faunas advantages of using fluvial cichlid fishes for eco- morphological comparisons include: (1) a reasona- We relied on the collection records of Winemiller ble preliminary hypothesis of phylogenetic rela- (1990,1991b, and unpublished data filed at the Texas tionship between and within cichlid faunashas been Natural History Collection, Austin) from numerous proposed recently (Stiassny1991), (2) for compara- locations within each of three river basinslocated in tive purposes,many functional morphological stud- separate biotic regions: South America, Central ies have been conducted on the feeding of cichlid America, and Central Africa (Fig. 1). To verify that fishes and similar percomorphs, (3) relevant all known cichlid specieshad been captured in each morphological characters and analytical methods drainage, we referred to Bussing (1987) for Costa for faunal comparisons have been established, and Rica, Bell-Cross & Minshull (1988)for Zambia, and (4) we have an extensive and reasonably detailed records in the Museo de Zoologia in Guanare, Por- ecological dataset for these ecologically diverse tuguesa for Venezuela. Our collections uncovered fishes. In addition to revealing a number of regular one previously undescribed cichlid species,Serra- features in patterns of faunal niche diversification, nochromis altus, in the Upper Zambezi drainage we demonstrate numerous ecomorphological con- (Winemiller & Kelso-Winemiller 1991). vergencesamong all
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