Evolutionarily Significant Units Among Cichlid Fishes: the Role of Behavioral Studies

American Fisheries Society Symposium 17:227-244. 1995 © Copyright by the American Fisheries Society 1995

Evolutionarily Significant Units among Cichlid Fishes: The Role of Behavioral Studies

Jay R. Stauffer, Jr. and N. J. Bowers1 School o f Forest Resources, The Pennsylvania Slate University University Park, Pennsylvania 16802, USA

K e n n e t h R . M c K a y e Appalachian Environmental Laboratory. University of Maryland Frostburg, Maryland 21532. USA

T hom as D . K o c h e r Department of Zoology, University of Sew Hampshire Durham, .Wew Hampshire 01823, USA

Abstract.—Cichlid fishes represent an outstanding case of explosive evolution and offer extraordi nary opportunities to investigate the evolutionary processes that have led to such diversity. Throughout the world, however, these fishes are threatened by overfishing, introduction of exotics, habitat destruction, and pollution of the environment. Determination of the specific status of local taxonomic units is critical for the development of programs both to conserve and to utilize these fishes for food, tourism, disease control, and scientific investigations. Rapid speciation within these fishes, however, has resulted in a paucity of characters for discriminating among species. Our experiences in Africa and Central America demonstrate that in situ behavioral studies, integrated with morphological and genetic analysis of taxonomic units, are vital to determining the specific status and relationships among evolutionarily significant units (ESUs). The critical element in determining whether a taxon is an ESU is knowledge of its reproductive biology; therefore, it is imperative that we develop a multidisciplinary emphasis in biodiversity studies.

The phrase evolutionarily significant unit (ESU) small disjunct population in the Monongahela implies that (1) a heritable difference exists among River system in West Virginia. Maryland, and populations; (2) an important statistical difference Pennsylvania (Stauffer et al. 1995). If this disjunct exists in a group of characters among units: and (3) population were designated as an ESU. then per a classification system is being used. From a pure haps a vehicle would be in place to protect this conservation point of view, any such ESU must be unique population of a widely dispersed species. protected. We are not suggesting that the term ESU Minimally, an ESU may be a population that replace our concept of a species or other formally exhibits a distinctive behavior. The importance of recognized taxonomic category but that it be used behavior in distinguishing among fish taxa was pio to recognize unique entities that need protection. neered by Trewavas (1983), who used behavioral For example. Waples (1991) suggested that a pop characters when delimiting three genera of tilapiine ulation should be considered an ESU if it is repro- fishes. In many cases, behavioral studies are instru ductivelv isolated from other conspecific popula mental in recognizing novel entities, assigning pop tions and if it represents an important component in ulations to taxa (Brooks and McLennan 1991), and the evolutionary trajectory of the species. Evolu estimating phylogenetic relationships among taxa tionarily significant units may also be defined geo (Wenzel 1992; deQueiroz and Wimberger 1993). graphically. in that they may be a particular com Nowhere is the designation and protection of munity or ecosystem that harbors a highly diverse ESUs needed more than in tropical ecosystems. It is fauna or flora or is a site of high endemism. Por estimated that as many as half of the extant species tions of a widespread population that has a disjunct inhabit the approximately 6% of the earth covered distribution may be designated as an ESU. For with tropical rain forests (Myers 1988). With re example, the longnose sucker Catostomus catosto- spect to fishes, there are 66 families endemic to mus (Forster) is panmictic; however, there exists a tropical freshwaters, whereas only 18 are endemic to temperate freshwaters (Berra 1981); moreover,

‘Present address: Environmental Sciences and Re greater than 70% of the described species of fishes sources. Portland State Universitv, Portland. Oregon inhabit the tropics (Moyle and Cech 1988). One of 97207. U SA the most speciose families of freshwater fishes is the STAUFFER ET AL.

Cichlidae. thus many of the examples that follow cal separation, ethological isolation, and allochronic will be from this family. mating. The development of many premating bar riers are the direct consequence of changes in be Species Concepts havioral characters. Several investigators have suggested that specia In part, the concept of the ESU involves grouping tion of cichlids may have occurred svmpatrically as individuals or populations into distinct taxa. which, well as allopatricallv (Fryer and lies 1972; McKave in tum. depends on the definition of species or et al. 1990). In svmpatric speciation models, repro some lower hierarchical taxon. Subsequent to the ductive isolating mechanisms originate within the evolutionary synthesis (Mavr 1982a: Eldridge 1985) dispersal area of the offspring produced by a single there has been much debate concerning species deme (Hartl and Clark 1989) and premating isola concepts (e.g., Simpson 1961: Wilev 1981: Donog- tion develops before populations inhabit distinct hue 1985: Paterson 1985; Templeton 1989: Mayr niches (Bush 1975). Controversy over the mecha 1992: van Devender et al. 1992). This debate can be nisms of svmpatric speciation center around the attributed to a certain degree to some biologists question of how reproductive isolation can arise treating species as epiphenomena. whereas others prior to a barrier to gene flow (Mayr 1982b). Koss- regard species as participants in the evolutionary wig (1963) suggests that populations can be isolated process (Mayr and Ashlock 1991). We would agree ecologically without oven geographical barriers, with Mavr (1992) that a nondimensional (nonhis- due to differences in habitat preference in a varied torican concept of the species is the one with which environment. Factors that may contribute to eco most biologists are concerned and which is probably logical isolation of populations include competitive the most applicable to conservation and protection isolation (McKave 1980). seasonal isolation (Lowe- programs. We argue, however, that it is difficult to McConnell 1959), mate selection isolation (Trewa- develop an unambiguous species definition given vas et al. 1972: Barlow and Munsev 1976). and the mixture of conspecific populations, incipient runaway sexual selection (Dominev 1984: McKave species, and good species that predominate in allo- 1991: McKave et al. 1993). In addition, intrapopu- patric populations of freshwater fishes, such as the lational variation in the expression of a given geno cichlids. Hence, the ESU provides an effective con type due to environmental conditions permits the cept upon which to base conservation practices maximum use of a heterogenous habitat (Liem and when dealing with rapidly evolving groups, such as Kaufman 1984; Via and Lande 1985). Within the the cichlids. cichlids, alternative adaptations (polymorphisms) may also have contributed to the extensive adaptive Speciation radiation and sympatric coexistence of closely re The concept of speciation involves the origin of a lated forms (West-Eberhard 19S3). unique gene pool. The processes responsible for the Cichlid fishes throughout the tropics and specif ecological separation and reproductive isolation of ically in the Great Lakes of Africa are generally populations have long been debated. Intralacustrine recognized as one of the most dramatic examples of allopatric speciation has been widely purported to extensive trophic radiation and explosive specia account for the rapid and extensive speciation by tion. Discrimination among species of Cichlidae can cichlid fishes in the African Great Lakes (Fryer be difficult because differences among species may 1959: Fryer and lies 1972: Mayr 1982b). The first be very small and intraspecific variation may be stage in allopatric speciation is geographical segre relatively large (Fryer and lies 1972: Ribbink et al. gation of a single population into two or more 1983). The acquisition of reproductive isolation subpopulations. Speciation culminates with the de without significant morphological change makes it velopment of reproductive isolating mechanisms difficult to distinguish African haplochromine cich that prevent interbreeding even if the geographical lids (Lewis 1982). Attempts to use starch gel elec barriers are removed and the populations experi trophoresis have been inconclusive for delimiting ence secondary contact (Mayr 1942). Both pre- and species (Komfield 1974. 1978). McKave et al. postmating isolating mechanisms influence repro (1982) electrophoreticallv examined three color ductive isolation among heterospecific populations. morphs of Peirotilapia triilentiger Trewavas (a cichlid Postmating isolating mechanisms include gametic endemic to Lake Malawi) that could not be distin mortality, zygotic mortality, hybrid inviability, and guished morphometricallv. They found no fixed al hybrid sterility; premating isolating mechanisms in leles at any of the 25 loci studied, although allele clude incompatible reproductive anatomy, ecologi frequencies were heterogeneous among taxa. sug- BEHAVIORAL STUDIES OF CICHLID FISHES 229

jesting that the color morphs represented isolated Sexual Selection gene pools or incipient species. Marsh (1983) sub Both natural and sexual selection have contrib sequently described these morphs as distinct spe uted to speciation within Cichlidae. The frequently cies. conflicting forces of natural and sexual selection Mitochondrial DNA (mtDNA) has been widely were first noticed by Darwin (1871). Natural selec recognized as an important tool for resolving rela tion arises from differential viability and fertility, tionships among closely related species. Mitochon whereas sexual selection results from differential drial DNA has also been used to delimit higher mate acquisition. In effect, a particular male trait taxonomic categories. Meyer et al. (1990) used can be a handicap in terms of survival but result in ntDNA sequence divergence to demonstrate the more fertilizations (Trivers 1972: Nur and Hasson nonophvly of the Lake Victoria cichlid species 1984). Sexual selection pressures can shift mean (lock, and Meyer et al.'s data suggest the possible male character values far from their equilibria at monophvly of the Lake Malawi flock. Monophvly of tained under natural selection alone (Kirkpatrick the Lake Malawi flock has been implied by mor and Ryan 1991). Although sexual dimorphism can phological studies (Stiassnv 1981) and supported by arise from other causes (Lande 1980: Hedrick and additional mtDNA analyses (Kocher et al. 1993). Temeles 1989), it is often a useful indicator of the Moran et al. (1994) conducted studies of phyloge magnitude of sexual selection acting on a character. netic relationships among African cichlids by means Commonly observed dimorphisms in body size, of restriction fragment length polymorphism plumage, coloration, or weaponry can often be as i RFLP) analysis of mtDNA. Recent work based on cribed to this force. DNA sequencing indicates that mtDNA may be In a recent review. Kirkpatrick and Ryan (1991) adequate for discriminating among Lake Malawi classified models of female-choice selection accord cichlids in some lineages (Bowers et al. 1994). Mo ing to whether selection on preferences was direct ran and Komfield (1993) caution, however, that the or indirect. They concluded that in many species rapid speciation of Malawian cichlids may have pre preferences evolve in response to direct selection vented sorting of mitochondrial lineages, allowing on female fitness. For example, female convict cich distantly related species of Lake Malawi cichlids to lids. Cichlosoma nigrofasciaium (Gunther) consis share mtDNA polymorphisms derived from a com tently prefer larger males when given a choice be mon ancestor. These results suggest that mtDNA tween two mates (Noonan 1983: Keenlevside et al. data alone cannot delimit certain Lake Malawi taxa. 1985). This preference may be interpreted as direct Detailed behavioral studies, however, have con selection for reproductive success because larger males provide better defense and resources for the sistently proven useful in distinguishing among spe young. Female preferences for males with larger cies. Many morphologically and genetically similar nuptial gifts (Thornhill and Alcock 1983) or for species can be separated based on breeding colora those carrying a lower load of a communicable tion and behavioral characteristics (Ribbink et al. disease (Borgia and Collis 1990) have a direct pos 1983: Witte 1984; McKaye and Stauffer 1986; itive effect on female fitness. Stauffer 1988: Stauffer and McKaye 1988; Stauffer Several models can be classified as invoking indi and Bolts 1989: Stauffer et al. 1993). Holzberg rect sexual selection on male and femaie prefer (1978) and Schroder (1980) first used behavioral ences. In the ‘‘good genes” models, female prefer observations to conclude that the blue-black color ence is derived from the improved fitness of a form of Pseudoiropheus zebra (Boulenger) was re- female's progeny because of genes acquired from productivelv isolated from the blue color morph the male. One such model postulates that females Pseudoiropheus callainos Stauffer and Hert (Pseudo- prefer males carrying genes that make those males rropheus abbreviated as P. hereinafter). That many resistant to parasites (Hamilton and Zuk 1982).. cichlid species, when artificially crossed under lab Conversely, "nonadaptive” models have been oratory conditions, can produce viable hybrid off postulated in which female preference is not related spring forces the taxonomist to rely solely on the to the forces of natural selection acting on the study of premating isolating mechanisms when de population. Hen (1989) demonstrated that the egg limiting species. Thus, behavior plays a significant spots of male Astatotilapia elegans Trewavas could role in defining svmpatric species and is essential in stimulate spawning and that female P. aurora Bur inferring whether or not allopatric species would gess spawned more frequently with males possess potentially exhibit reproductive isolation. ing higher numbers of egg spots (Hert 1991). Fisher 230 STAUFFER ET AL.

(1930) was the first to propose a “runaway” process, may lead to assortative mating of populations prior which has since been extensively modeled (O’Donald to a sympatric speciation event or during secondary 1980; Lande 1981; Kirkpatrick 1982) and discussed contact following allopatric speciation; thus, one or (Arnold 1983; Kirkpatrick 1987). One feature in the several sexually selected traits may become differ nonadaptive models is that the runaway process can entiated with each speciation event. Strong sexual be initiated by arbitrary female preferences, and selection may cause differentiation of breeding be several recent studies have shown that female pref haviors even in the face of considerable gene flow erence for particular male characters can evolve and among diverging populations in secondary svm- long before the characters themselves. Basolo patry. Natural selection may act to differentiate (1990, 1991) demonstrated a preexisting preference morphological and behavioral traits further. There for caudal swords in swordl^ss species o f the poeci- fore. it is our contention that the use of both mor liid Xiphoplionis. Meyer et al. (1994). however, pro phological and behavioral data to delimit closely vided genetic evidence suggesting that the ancestor related species, such as the Lake Malawi cichlids. is of this genus possessed a sword. Preferences may essential. Below we discuss the use of color, bower frequently arise from sensory biases (Ryan and shape, courtship behavior, and feeding behaviors to Keddv-Hector 1992) and may be an inherent prop discriminate among cichlid species. We consider erty of sensory systems (Enquist and Arak 1993). color form and bower shape to be manifestations of Kirkpatrick and Ryan (1991) interpret this to mean behavioral characteristics via female choice. In that direct selection was responsible for the evolu many cases, behavioral studies may first identify tion of female preferences. Ryan and Rand (1993) novelties that indicate which specific forms might be have stressed the importance of recognizing that valid species. sexual selection and species recognition are ele ments of a single process: the matching o f male Case Histories Demonstrating the Value of signal traits to female preference function. Behavioral Studies The existence of speciose flocks of animals re Role of Color in Delimiting Species stricted to isolated habitats may best be explained by sexual selection in many cases. The large number The incredible variety of color patterns within the of Drosophila species endemic to Hawaii led Ringo haplochromine cichlids of the African Rift lakes is (1977) to elaborate on the hypothesis of Spieth well known (see Figures la-f: Fryer and lies 1972: (1974) that sexual selection can accelerate the di Greenwood 1981; Ribbink et al. 1983: McKaye and vergence of populations. Carson (1978) suggested Stauffer 1986), and we consider it to be essential in that sexual selection could create coevolutionary female mate selection. The existence of unique races between particular male characters and fe color patterns is recognized to be suitable for de male preferences, leading to the evolution of in limiting species (Barlow 1974; Barel et al. 1977: creasingly complex courtship behaviors. Possible in Greenwood 1981; Hoogerhoud and Witte 1981: teraction of founder effects and sexual selection McKaye et al. 1982'. 1984), and in many cases new during speciation was suggested by Kaneshiro species have been recognized solely on the basis of (1989) as an explanation for the Drosophila species male color pattern (McElrov et al. 1991). Although flock. Dominey (1984) generalized these hypotheses coior is certainly a morphological character, we re to account for rapid speciation in African cichlids gard it as a manifestation of female preference, and recognized that the cichlids share many char which is a behavioral trait. acteristics with the Hawaiian Drosophila, including The following rock-dwelling (mbuna) taxa were sexual dimorphism, lek-based breeding systems in first hypothesized to be valid species based on male voking a high degree of female choice, and isolated breeding color and later substantiated based on local populations. morphometries and meristic data: P. aurora (Bur We propose that the variations observed in male gess 1976), P. barlowi (McKaye and Stauffer. 1986). coloration, bower size (breeding platform), and P. flavus (see Figure la), P. ater, P. cyanus (Stauffer courtship behavior among closely related cichlid 1988), P. xanstomachus (Stauffer and Boltz 1989). species are the result of intraspecific sexual selec and P. callainos (Stauffer and Hert 1992), among tion (McKaye 1991). In many instances, morpho others. logically similar populations may in fact be subspe Holzberg (1978) and Schroder (1980) demon cies, sibling species, or incipient species at various strated that color patterns of females may also be stages of speciation (Mavr 1963). Divergence in useful in delimiting species, such as within the P. female preference for male secondary sexual traits zebra species complex. Male P. callainos are pale HI IIAMORAL STUDIES OF CICHLID FISHES 231

>m iho Jiverse color patterns exhibited In Lake Malawi cichlid*': riUif>ui c.f. rliodcui :rom Kanjcdza 1

232 STAUFFER ET AL.

0 .1 8

m « £ 0.12 L o E o a. 0.06 k . O s 0 - CM o Q. ■g -0.06 - h. nj o

-2.14 -1.6 -.08 0 0.8 1.6 PC1 (Meristics)

F ig u r e 2.—A plot of the second principal component (PC2: morphometries) and the first principal component (PC 1: meristics) based on data from P. catlainos and P. c.f. zebra ‘mazinzi."

blue (Stautfer and Hert 1992) and closely resemble stant characters to define them. To regard them as an undescribed P. c.f. zebra from Mazinzi Reef. more than one species meant only to limit the num Lake Malawi. Many female P. callainos are white, ber of material at hand, and so I have lumped them whereas white females of P. c.f. zebra from Mazinzi all in one." Three species of this group are presently Reef have never been collected. This observed dif recognized by Barlow and Munsey (1976), although ference in female color pattern prompted us to Villa (1982) only recognized two. Our behavioral complete a more detailed morphological study of work, however, confirms that the three species rec these two forms. Based on sheared principal com ognized by Barlow and Munsey (1976) are, in fact, ponent analysis of morphometric data and principal valid. Furthermore, our direct underwater observa component analysis of meristic data (see Stauffer tions that these forms assortativelv mate by color 1993 for an explanation of the methods employed), and that their habitat preferences and nest forms the two taxa were shown to be heterospecific (Fig differ suggest that at least three additional unde ure 2). scribed species are also present. Preliminary mor The importance of color pattern is not limited to phological analyses of two of these forms (Figure 4) the haplochromine fishes in the Great Lakes of confirm that they are distinct from the type speci Africa. Our work over the past 3 yean throughout mens housed in the Natural History Museum (Lon the Great Lakes basin in Nicaragua has impressed don). upon us, as it has earlier workers (M eek 1907; Similarity in color patterns, however, may be mis Barlow and Munsey 1976), the great variation leading. For example, many authors (e.g.. Fryer and among cichlids in coloration and body form in iso lies 1972; Ribbink et al. 1983) regard the two pop lated water bodies (see Figures 3a-c). For example, ulations of the Lake Malawi blue-black (BB; Figure in the midas cichlid Cichlasoma citrinellum group, Id) color form of P. zebra at Nkhata Bay and several species have been described. With respect to Thumbi West Island to be conspecific. McKave et this commercially important group of cichlids. al. (1984) found differences in allele frequencies Meek (1907:122) stated, “Of all the species of fishes between northern and southern populations of BB in these lakes, this one is by far the most variable. I P. c.f. zebra although there were no fixed allelic made many repeated efforts to divide this material differences. Examination of the morphological data ... in from two to a half-dozen or more species, but (Figure 5) suggests that these two populations are in all cases I was unable to find any tangible con actually heterospecific. Another example includes c.

F ig u re 3.— Representatives «»i the 'pecio cnnmicx **i :ne midas cichlid Cichlasoma citrinellum Gunther, (a) Cichlasoma c.f. citrinellum "\il«»a" fr»*111 l .i^nm vie \iU»a. Nicaragua: il>» Cichlasoma c.f. citrinellum “am arillo” from Laguna de Xiloa. Nicaragua: ;nul 1 0 < iiltiuw ht c.t. • :mn< "chanclio" from Laguna de Apoyo, Nicaragua. 234 STAUFFER ET AL.

3 r

- 2 ------0.3 -0.2 -0.1 0 0.1 0.2 0.3 0.4 PC1 (Meristics)

F ig u r e 4.— A plot of the sheared second principal component (PC2: morphometries) and the first principal component (PCI: meristics) based on data from three members of the Cichlasoma cimnellum species group: Cichlasom a cim n ellum type material from the British Museum (Natural History). C ichlasom a c.f. cininellum "grenada" from Lake Nicaragua, and C ichlasom a c.f. cininellum "Xiloa" from Laguna de Xiloa.

the orange blotch (OB) morphs of many Lake Stauffer (1993) described this form as a single spe Malawi cichlids (e.g. P. zebra, Labeotropheus tre- cies. Melanochromis heterochromis Bowers and wavasae Fryer [see Figure lb], and P. rroplieops Stauffer (Figure lc). Regan). Color differences would initially suggest Color pattern may also provide insight into the that these forms are heterospecific with the simi phvlogeny of certain groups, although care should larly shaped, normally colored individuals: however, be taken when interpreting the results. For exam closer examination shows that all OB morphs are ple. the prevalence of the BB color morph in most female, suggesting that these color forms are not of the rock-dwelling cichlid genera (see Figure valid species. ld-e) and some sand-dwelling forms (Figure If) Color differences in allopatric populations may throughout Lake Malawi suggests that this color also be misleading. For example, two populations of pattern is primitive, whether one uses the common a Melanochromis species occur at Chinyamwezi and ality principle or outgroup comparisons (Smith and Chinyankwazi Islands in Lake Malawi. Because Koehn 1971; Watrous and Wheeler 1981). Con male coloration differed between the two popula versely, the presence of the red dorsal fin within P. tions, Ribbink et al. (1983) regarded these taxa to c.f. zebra “red dorsal,” P. c.f. zebra “cobalt mbenji." be heterospecific. Examination of the morphomet and Labeotropheus trewavasae implies that this char ries and meristics of 13 populations of this form acter state is a product of convergent or parallel from other locations within Lake Malawi revealed evolution. slight clinal variation in shape pattern (Bowers and In their recent monograph of non-mbuna haplo- Stauffer 1993), suggesting that these populations chromines endemic to Lake Malawi, Eccles and. are conspecific. This conclusion was supported by Trewavas (1989) suggested that similarity of color allozyme analysis, which showed very low variation patterns among species may reflect phyletic rela at 3 polymorphic loci out of 24 loci that were as tionships. For example, the “polvstigma” pattern, sayed. Because the morphological evidence indi which consists of three longitudinally arranged fea cated no differences in shape among the popula tures of either stripes or a series of spots or tions, and variation in male coloration tended to be blotches, is restricted to the genus Nimbochromis greater within than among populations. Bowers and (Figure 6d). Conversely, the following melanin pat BEHAVIORAL STUDIES OF CICHLID FISHES 235

PC1 (Meristics)

Figure 5.—A plot of the sheared second principal component (PC2: morphometries) and the first principal component (PCI; meristics) based on data from two populations of the blue-black color form of zebra mbuna P. zebra from Nkhata Bay (northern population) and Thumbi West Island (southern population). Lake Malawi. Malawi.

terns are found in more than one genus: “kirkii” upper lateral line: and “rostratus” pattern (Figure pattern (Figure 6a), which emphasizes the horizon 6g), which consists of three series of large spots tal elements of the very common and hence perhaps approximately in the position of the stripes or rows pleisiomorphic color pattern, is represented by that constitute the kirkii pattern, is represented by Syassachromis breviceps (Regan), Lethrinops lethri- Fossochromis rostratus (Regan) and Eclectochromis nus Gunther, and Protomelas kirkii (Gunther); trans festivus (Trewavas). Consequently, Eccles and Tre verse bars (Figure 6b), is represented by Placidochro- wavas (1989) considered the rostratus color pattern mis johnstoni (Gunther), Lethrinops gossei Burgess a result of parallelism and thus uninformative. and Axelrod, and Alticorpuspeterdaviesi (Burgess and Axelrod); “dimidiatus” pattern (Figure 6c), which is a Role o f Bower Shape in Delimiting Species simple, straight, midlaterai band, is represented by Dimidiachromis dimidiatus (Gunther) and Taenio- Research on the breeding behavior of several chmmis holotaenia (Regan); oblique band (Figure 6e), Lake Malawi sand-dwelling fishes has demonstrated which consists of an oblique band or series of spots that the process by which females choose mates is from nape to middle of the caudal base, is represented complex. McKaye et al. (1990) found a preference by Docimodus evetynae Eccles and Lewis, Mylochromis for males with larger bowers in female Copadichro anaphyrmus (Burgess and Axelrod), and Taeniolethri- mis conophorus Stauffer, LoVullo, and McKaye. nopspraeorbitalis (Regan); three-spot patterns (Figure Males of this species form huge leks that may have 6f), which consists of a series of spots that appear more than 50.000 males at the height of the breed along the position of the midlateral component of the ing season (McKaye 1983, 1984). In comparisons horizontal element of the plesiomorphic pattern, is between paired bowers, males on larger bowers represented by Otopharynx ovatus (Trewavas) and received a two- to threefold increase in female at Copadichromis quadrimaculatus (Regan), which tention (bower entry and circling behavior) over have the spots below the upper lateral line, and males on smaller bowers. In a smaller lek occupied Cyrtocara moori Boulenger and Ctenopharynx pictus by 20 to 50 Otopharynx argyrosoma (Regan) males, (Trewavas), which have the spots above or on the the males occupying bowers closest to the center of 236 STAUFFER ET AL.

F ig u r e 6.— Examples of the color patterns recognized by Eccles and Trewavas (1989) as being phylogeneticallv informative for Lake Malawi cichlids: (a) kirkii pattern, (b) transverse bars, (c) dimidiatus pattern, (d) polvstigma pattern, (e) oblique band, (f) three-spot pattern, and (g) rostratus pattern.

the lek received approximately three times as many In Lake Malawi, 10 major bower forms, which matings as did the males around the periphery vary in size from small depressions in the sand to (McKaye 1991). In order to separate the effect of elaborate castles, have been identified (McKaye bower size and bower location, we substituted arti 1991). Within each class of bower shape, significant ficial bowers in the lek of Lethrinops c.f. parvidens quantitative variation in bower dimensions occurs. (Trewavas). Several tagged males located on the Among bowers within a lek, height varies depend periphery of the lek had not been observed to fer ing on the age of the bower and the activities of the tilize any eggs during a 3-week period during which male. Some dimensions of the bower remain con approximately 1,800 eggs were laid in other areas of stant, despite variation in height, strongly suggest the lek. The same tagged males were observed fer ing a genetic basis to bower form. The diameter of tilizing between 15 and 30 eggs per day when large the breeding platform of the bowers of Copadichro- (approximately 22 cm in height) bowers were placed mis conophorus appears to be species specific on top of the tagged males existing ones. In another (Stauffer et al. 1993). We demonstrated that three arena, female Lethrinops aurinis (Regan) preferred closely related species in the Copadichromis euci- to mate with males whose bowers contained more nostomus group had differently shaped bowers, and peripheral bumps. In general, these data suggest we used these data to aid in the differentiation of that within several species, a specific character, these species. Similarly, McKaye et al. (1993) stud bower size, can influence the mate preference of ied five leks of Tramitichromis near Nankumba Pen females and that males will evolve behaviors that insula in Lake Malawi and demonstrated significant increase the size, shape, or position of their bower differences in bower shape among these leks. These in order to attract more females. data are discussed in more detail in the section 236 STAUFFER ET AL.

0 .0 6

Brine Shrimp 0.04

a. 0.02 - -o x>

- 0.02 - z

-0.04 -0.12 -0.08 -0.04 -0.0 0.04 0.08 0.12 Sheared PC2

Figure 7.—A plot of the second and third sheared principal components based on eight head measures collected from a split brood of P. c.f. zebra ‘red-top" fed two different diets.

the effects of diet on the phenotype of two New pharyngeal bones and larger molariform teeth than World cichlids: a mouthbrooder. the redhump did those individuals that ate snails with thinner eartheater Geophagus steindachneri (Eigenmann shells. In preliminary experiments conducted in our and Hildebrand), and a substrate spawner, the pearl laboratory, we used F, siblings derived from wild- eartheater Geophagus braziliensis (Quov and Gai- caught P. c.f. zebra “red top" and randomly divided mand). The experimental design was similar to that them into two dietary treatments: (1) brine shrimp of Meyer’s (1987) and both species exhibited the nauplii and Daphnia magna and (2) commercial expected trend. Based on this study it would appear flake food and tubifex worms. After 18 weeks the that mouthbrooding may not greatly alter the phe fish were sacrificed and morphometric measure notypic plasticity induced by diet in substrate- ments were recorded. A sheared principal compo spawning cichlids. nents analysis, in which cheek depth, head depth, Similar studies have not been conducted on Old and snout length accounted for most of the variabil World cichlids, but there have been some important ity, resulted in complete separation of the two observations. Witte (1984) reported that wild- groups (Figure 7). caught (Lake Victoria) and domesticated Haplo- Clearly, approaches integrating morphological, chromis squamipinnis Trewavas had differently genetic, ecological, and ethological data are re shaped premaxillaries. The difference was attrib quired for species-level description of these fishes. uted to the fact that those individuals kept in In a study of five putative populations of Trami- aquaria dug in the sand with their mouths, thus tichromis species in the vicinity of Nankumba Pen increasing the power of their bite over that of the insula in Lake Malawi, McKaye et al. (1993) exam wild-caught ones, which did not exhibit this digging ined protein electromorphs of 24 enzyme loci and behavior. In addition, Witte (1984) noted that the compared these data with bower shape of each of change in premaxillarv shape was not limited to the five populations. No fixed differences were young fish, indicating that it was not strictly con found for any of the alleles. Frequency differences trolled by some ontogenetic factor. A second im indicated that the two populations found at Cape portant observation was reported by Greenwood Maclear were distinct from the populations from (1965) for Astatoreochromis alluadi Pellegrin. Indi Kanjedza Island, Mpandi Island, and Nkudzi Point. viduals feeding on thick-shell snails had stronger The population inhabiting Nkudzi Bay, which is

4 J BEHAVIORAL STUDIES OF CICHLID FISHES 239

located between Kanjedza Island and Mpandi Is Taslh I.—Distribution of mitochondrial DNA haplo- land was intermediate between these islands and types among four populations of Copadichromis once sus the populations at Cape Maclear. Shape analysis of pected to be conspecific. All populations are from south bower forms produced two major groupings, which ern Lake Malawi. showed that the bowers from populations located at Mitochondrial DNA hapiot>pes Cape Maclear were distinct from those found at the Population A B C D E F G H I

other three localities. A critical examination of the Thumbi West Island 16 3 0 0 0 0 0 0 0 lower pharyngeal bone and the gill rakers located Cape Maclear 1 II 0 4 T 1 0 0 0 on the ceratobranchial showed that populations Kunchedza Island 0 0 14 I 0 0 : o 0 Mazinzi Reef 2 j 0 -> 1 0 0 1 3 from Nkudzi Bay, Mpandi Island, and Kanjedza Island were Lethrinops c.f. parvidens. whereas those located at Cape Maclear were Tramiiichromis c.f. lituris. Hence, the results suggested by the morpho tectable behavioral differences may have initiated logical. genetic, and behavioral data were congru the speciation process through assortative mating, ent. which may. in turn, lead to runaway sexual selec Another example of congruence among genetic, tion. Thus, behavioral data are extremely valuable morphological, and behavioral data is found in the and. at least with some groups such as cichlids. are three species Copadichromis conophoros. C. cycli- essential and can (1) initially identify distinct taxa or cos. and C. rhinos, which were recently described by identify novelties which prompt further investiga Stauffer et al. (1993). For over a decade, extensive tion: (2) confirm or support genetic and morpho research on the ecology and behavior of these sand- logical data needed to delimit taxa: and 13) provide dwelling fishes indicated that at least three popula needed information to speculate on phytogenies. tions. which fit the original description of Copadi It is our contention that if ESUs are recognized at chromis euctnostomus. constructed bowers with the population level, the population designated three different population-specific shapes. The clus should possess some heritable atypical trait, such as ters formed by plotting the principal component an unusual behavior pattern. Perhaps an ESU can analysis scores (see Humphries et al. 1981 and be designated on a temporary basis because of an Bookstein et al. 1985 for a discussion of shape unresolved txxonomic status. We are not proposing analysis) of the morphometric and meristic data for that the ESU replace existing taxonomic categories Copadichromis conophonis and C. cyclicos did not but that these units be given standard nomencla- overlap. Copadichromis thinos. although intermedi tural status when possible, so that they are formally ate. was significantly different (P < 0.05) from the recognized by the scientific community. Such dis other two species. Shape analysis also confirmed tinction provides the necessary framework to ini that bower shapes for the three species were signif tiate and foster debate on the significance and re icantly different (P < 0.05), although data from the ality of such discrimination. We realize that species bowers of Copadichromis conophorus were interme definitions and concepts are difficult and sometimes diate. Subsequent to the description of these taxa. burdensome, but we urge investigators not to re mtDNA haplotype frequencies in Copadichromis gard these varied concepts as mutually exclusive. conophorus. C. cyclicos. C. thinos. and an unde We also conclude that behavioral data are essential scribed species of Copadichromis from Thumbi to delimit species. West Island were examined (Table 1). Haplotype We further propose that the ESU be defined in frequencies were significantly different (P < 0.05) geographical terms, so that areas of high diversity or among populations. Males on the small lek at endemism can be designated as ESUs. Such a unit Thumbi East Island are nearly fixed for a single may consist of crater lakes in Nicaragua or partic mtDNA haplotype. These data confirm the genetic ular islands or shorelines in Lake Malawi. For ex uniqueness of Copadichromis conophonis. C. thinos. ample. in the southeast arm of Lake Malawi more and C. cyclicos. which had been inferred from mor than one-third and one-half of the species native to phological evidence. the Maleri Islands and to Chinyankwazi and Chinv- amwezi Islands, respectively, are endemic (Figure 8). Such a geographical approach to conservation Conclusions must permit the continued use of the lake by In sympatric situations behavior can provide di Malawians, who derive about 70% of the animal rect evidence for reproductive isolation or cohesion. protein consumed from fish, and must also preserve In both allopatric and sympatric circumstances, de- those areas that harbor high concentrations of ge- 1

240 STAUFFER ET AL.

0 Chinyamwezi and

° Chipyankwazi Is. Maleri Is

Mumbo I Domwe (20/4) Tanzania Zambia Thumb! West I, o Thum&i East I. (23/0) ' Kanchedza I. (17/0) Lake, Nankumba Malawi P en in su la

M ozam bique

F ig u r e 8.—A map of the southern region of Lake Malawi showing the total number of species of mbuna at a given location and the number of those species that are endemic to the location.

netic diversity. As stated by Orville Freeman References (former U.S. Secretary of Agriculture), “We make a Arnold, S. J. 1983. Sexual selection: the interface of the potentially dangerous mistake when we assume that ory and empiricism. Pages 67-108 in P. Bateson, ed we must choose between serving humanity or serv itor. Mate choice. Cambridge University Press. Cam ing the environment. It must be a priority to bring bridge, Massachusetts. these goals into harmony. They need not and they Atchley, W. R. 1971. A comparative study of the causes must not be mutually exclusive.” and significance of morphological variation in adults and pupae of Culicoides: a factor analysis and multi ple regression study. Evolution 25:563-583. Acknowledgments Baltz, D. M., and P. B. Moyle. 1981. Morphometric anal This work was funded in part by the U.S. Agency ysis of tule perch (Hysterocarpus traski) populations in for International Development Program in Science three isolated drainages. Copeia 1981:305-311. Barel. C. D. N., M. J. O. Van Oijen. F. Witte, and E. L. M. and Technology Cooperation, Office of Science Ad Witte-Maas. 1977. An introduction to the taxonomy visor (Grant Number 10.069, Com-5600-G-00-0017- and morphology of the haplochromine Cichlidae 00; Grant Number 11.204, DHR-5600-G-1043-00); from Lake Victoria. Pan A: text. Netherlands Journal the National Science Foundation (BNS86-06836; of Zoology 27:333-389. IBN-9225060; BSR-9007015); and Fulbright Re Barlow, G. W. 1961. Causes and significance of morpho search Awards (Council for International Exchange logical variation in fishes. Systematic Zoology 10:105- 117. of Scholars) to Jay Stauffer and Kenneth McKaye. Barlow, G. W. 1974. Contrasts in social behavior be The authors appreciate the critical review of the tween Central American cichlid fishes and coral reet manuscript by Deborah McLennan and Allan de surgeon fishes. American Zoologist 14:9-34. Queiroz. Barlow, G. W„ and J. W. Munsey. 1976. The red devii- BEHAVIORAL STUDIES OF CICHLID FISHES 241

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