Env. Biol. Fish. Vol. 8, No. 2, pp. 81-96, 1983

Ecology and breeding behavior of a fish, Cyrtocara eucinostomus, on a large lek in Lake Malawi, Africa

Kenneth Robert McKaye Duke University Marine Laboratory, Pivers Island, Beaufort, North Carolina 28516, U.S.A.

Keywords: Arena, Mouthbrooding, Sociobiology, Predation, Cape Maclear, Zooplankton, Cormorant, Bagrus meridionalis

Synopsis

Cyrtocara eucinostomus, a mouthbrooding cichlid, breeds on a 4 km long breeding arena between 3-9 m depth in the Cape Maclear region of Lake Malawi. At times over 50,000 males display there, making this breeding arena the largest ever reported. The form and function of the arena and the behavior of the fish on the arena are analogous to bird leks. This arena serves only as a mating ground. All parental care is provided by the females, which leave the arena with the eggs. Courtship takes place in the morning and most of the males leave in the afternoon to forage on zooplankton in deeper water. They return at dusk. The few males that remain on the arena switch their behavior from courting to foraging on zooplankton. Comparisons of this fish arena are made with bird leks and it is concluded that the mating system of this fish can be defined as a lek in the avian sense. 1) There is no male parental care and an absence of monogamous pair bonding. 2) Males and females are sexually dimorphic and there are males present which mimic females to gain entrance into the arena. 3) The arena is traditional with a lack of environmental constraints and is away from the primary feeding grounds. In order to determine 1) if this arena could be considered a true lek and 2) what the factors are which account for the location of this remarkably large arena in shallow water, data were collected upon: 1) the depth distribution of C. eucinostomus; 2) distribution and size of the nests on the arena; 3) the behavior of the fish on the arena; 4) the feeding habits of C. eucinostomus; 5) the distribution of the zooplankton upon which C. eucinostomus feeds; 6) water temperature throughout the year; 7) response of males to cormorants; 8) depth distribution and stomach analysis of predatory catfish which feed on C. eucinostomus. Based on this natural history data, it is concluded that the occurrence of the arena in shallow water is probably due to C. eucinostomus avoiding deep dwelling catfish which feed at night upon them and other .

Introduction McConnell 1969, Fryer & lies 1972, Baylis 1974, Barlow 1974, 1976, Brichard 1975, Balon 1977, Cichlid fishes exhibit a wide range of breeding M cKaye 1977, Keenleyside 1979, W itte 1981). The habits, varying from the biparental care of young latter reproductive mode is characteristic of most of for periods of over 2 months to uni-parental mouth­ the cichlid fishes of the Great Lakes of Africa. In brooding of young by either male or female (Lowe- Lake Malawi, the males of many of these cichlid congregate on spawning arenas (Fryer & Received 4.8.1981 Accepted 16.4.1982 lies 1972) for the apparent purpose of attracting

© 1983, Dr W. Junk Publishers, The Hague. Printed in The Netherlands. 0378-1909/83/0082-0081 /S03.20 81 and displaying to females. The eggs are both Malawi. The hypotheses to account for the selec­ fertilized in and retained in the female’s mouth and tion of this site by males of this species are: (1) it is a there is no male parental care of the young. The place where there is abundant food; (2) it has the females usually leave the arena, carrying their only suitable substrate; (3) competitors force them young for a while and release them elsewhere. Both into this area; (4) physical constraints, relating to the structure of the arena and the behavior of the temperature, oxygen or wave action make the site fish are considered analogous those seen in lekking atractive; 5) it is the area most secure from pre­ birds (Lack 1968, Fryer & lies 1972). dators. Lek-based mating systems are characterized by Data were collected on: (1) the depth distribution polygynous or promiscuous mating, weak or no of C. eucinostomus; (2) distribution and size of the pair-bonding, no paternal care and localized areas nests on the arena; (3) the behavior of the fish on where males and females congregate to mate (Se- the arena; (4) the feeding habits of C. eucinostomus; lander 1972, Wilson 1975). Males establish them­ (5) the distribution of the zooplankton upon which selves on the lek prior to mating (Beuchner 1961, C. eucinostomus feeds; (6) water temperature Snow 1963) and as a result of competition for throughout the year; (7) response of the males to females, a ritualized dominance hierarchy has usu­ cormorants; (8) the depth distribution and stomach ally evolved. Loiselle & Barlow (1979) consider that analysis of predatory catfish which feed upon C. ‘all the classic features of such avian leks may be eucinostomus. interpreted as manifestations of an hierarchical The natural history data presented here will be social structure’. used to discuss: (1) the extent to which this mating The evolution and adaptive value of lekking is system can be considered a lek, in the classical not well understood. Bird leks probably evolved ‘avian’ sense; (2) the factors which account for the from communal groupings (Crook 1965) where location of the remarkably large arena; (3) variation there existed competition for breeding sites as well in the form of the arenas in different areas in the as synchronous breeding (Selander 1972). Since leks lake. occur primarily in species inhabiting open country or having limited breeding areas (Loiselle & Barlow 1979), it is likely that they serve to concentrate Methods and materials widely distributed stocks of males and females. Loiselle & Barlow (1979) compare avian and fish Observations on the breeding behavior of C. eucino­ leks, and acknowledge some controversy exists over stomus were made underwater with open-circuit their use of the term ‘lek’ for many of the fish SCUBA from December 1977 to August 1980. breeding systems they discuss. To be considered a Counts, measures and general notes were made on ‘true’ lek, ornithologists require: (1) that the arena writing slates and transcribed after each dive. Indi­ serve only as a mating ground with the female vidual nest-holding males were observed for periods leaving to tend the young by herself and (2) the of 15 min at an average distance of 2-3 m, depend­ absence of habitat constraints in determining the ing on visibility. A total of thirty-four males were location or extent of the arena (Pitelka, in Loiselle watched between 0600 and 1300 h and nine dif­ & Barlow 1979). In Lake Malawi, Africa, the ferent males were observed from 1300 to 1900 h. breeding arenas of several cichlid species, including The number of foraging bites, mouthfuls of sand Lethrinops furcicauda, L. aurita and Cyrtocara moved to build nests, attacks and threats upon argyrosoma exhibit these classical characteristics of fishes and courting of females were recorded. Indi­ avian leks (personal observation). vidual egg-laying females were followed when over This report concerns the ecology and breeding the arena and the number of eggs laid and distance behavior of C. eucinostomus along a 4 km long, traveled throughout the lek were recorded. 3-12 m deep spawning arena off the Nankumba Peninsula in the Cape Maclear region of Lake

82 Abundance of C. eucinostomus and their nests: The the arena. The time an individual cormorant fished num ber o f C. eucinostomus and their nests were was recorded. The depth at which it fished was estimated by two divers counting the fish within 5 m determined from estimating the distance from the of the bottom and 2 m on either side of a 50 m shore and knowing the depth profile of the region. transect line laid along a depth contour (100 m2 of bottom surface for each diver). From November Collection o f C. eucinostomus for gonadal study and 1977 until July 1978 and in June and July 1979, at tagging: Both males and females were collected with least two 100 m2 surface transects were made each gill nets at various times on the breeding arena. The month at each 3 m depth interval, down to 32 m. gonads were examined and all the eggs were count­ The base diameter, top diameter and height of 15 C. ed. All of the eggs in the gonads of sixteen females eucinostomus nests (Fig. 1) were measured on 26 collected on 14-18 July 1980 were measured to the July, 1980 in Nkhata Bay (approximately 200 miles nearest 0.1 mm. The largest eggs of all fish were also north of the main study). On 29 July, 1980, 15 nests measured through a microscope, using an ocular were measured on the four kilometer arena. micrometer. Males were characterized as either ‘ripe,’ with large white testes, or 'non-ripe,' with Occupancy o f nests: During a 6 month period from small string-like testes. One hundred and twenty February-July 1978, the number of nests occupied males were tagged underwater with Dennison T and unoccupied were counted at various times tags and their standard lengths were measured. The throughout the day. The number of nests counted males were returned to their original nests after for each hour ranged between 104 and 444. If no tagging. male was seen attacking other males or building up the nest it was termed unoccupied. Counts were also Stomach analysis o f C. eucinostomus: Four collec­ made between 0700 and 1000 h when white-necked tions of C. eucinostomus were made on 2 and 16 cormorants, Phalacrocorax carbo, were feeding in February and 1 and 17 April, 1980. Cyrtocara

Fig. I. Male C. eucinostomus on nest.

83 eucinostomus feeds almost exclusively on zooplank­ the arena) and 8-10 m (in the arena) for eleven ton. Each individual plankter was counted in the nights in July and August 1980. Placed approxi­ stomachs of 120 fish, which had been preserved in mately 1 km apart, they were set between 1600­ formalin. The length of a sub-sample of up to 40 1800 h and retrieved between 0600-0800 h the individual plankters found in the stomachs of each following morning. The nets were alternated at each of 21 fish collected over the arena on 15-17 July, depth to eliminate the possibility of differential 1980, were measured. capture rates. The Bagrus and Clarias catfishes were collected from each net. Their standard lengths Zooplanton analysis: Starting in M arch, 1978, were measured and the stomach contents analyzed. zooplankton samples were taken weekly in 17 m of water approximately 60 m offshore from the Capture of the predatory catfish, Bagrus meridio­ study area (see McKaye, 1981, Fig. 1 for location). n a ls from between 1-60 m: 180 m of trammel net Samples were collected with a 9 1 Van Dorn Bottle were placed 3 July-20 August, 1980 at various and concentrated through a 64 /an net. Three depths throughout the Cape Maclear region. The samples were taken at depths of 5 m, 10m and 15 m depths of the deep ends were determined by sound­ and were combined to total 27 1 samples from each ing. The measure of depth used, ‘middle depth,’ was depth. Because of mechanical breakdowns and bad determined by averaging the depths of the shallow weather, it was not always possible to sample every and deep ends of the nets. The nets were set over week. The plankters were identified to species, night and the number of B. meridionalis captured Mesocyclops leuckarti, Mesocyclops neglectus, Tro- was recorded. Many of the fishes (catfish, cichlids, podiaptomus kraepelini, Thermodiaptomus mixtus, etc.) collected are deposited with the Smithsonian Diaphanosoma excisum. Juveniles and adults of Institution. each species were identified and counted separately; all nauplii were counted. For the purpose of this report, however, I will only present the data for the Results diaptomids and Diphanosoma excisum. They are the primary food of C. eucinostomus. The lengths of Distribution and size of nests: Cyrtocara eucinosto­ all the plankters collected on 17 July 1980 were mus bred from October 1977 through March 1981 measured. along the sandy northern shore of the Nankumba Peninsula. C. eucinostomus nests occurred along the Water temperature: Water temperatures were rec­ entire 4250 m length of this shore (see McKaye orded at either a station between W. Thumbi Island 1981, Fig. 1). and Domwe Island or above the arena. These were All of the shallow nests were between 1 -14 m depth, taken with a thermometer from water collected at with over 90% of them between 3-9 m (Fig. 2). The 5 m depths with a Van Dorn bottle. The data number of nests varied seasonally and appeared to presented here are for 0 m from November 1977— show a bimodal distribution, with the highest dens­ August 1980 and 5 and 10 m from March 1978 until ity, 0.5 -nT 2, occurring in January-April and again February 1980. in July-August. The estimated number of nests varies between 50,000 and 5,000 along the beach Transparency: Secchi disk readings were taken con­ (McKaye & Reinthal, in preparation). currently with the plankton samples from March The density of non-territorial fish within 5 m of 1978 through August 1980 just offshore from the the substrate followed a similar pattern as the nests. breeding area. The highest mean density was 1.80-m-2, between 3-6 m (Fig.2). Capture of predatory catfish near arena (8-25 m): Two 90 m trammel nets were placed parallel to the Nest size and spacing: Males built elevated mounds shoreline at depths of between 20-25 m (offshore of (Fig. 1) with average dimensions of: base diameter

84 N = 12 20 23 23 18 12 12 10 14 1980. A t N khata Bay, during July 1980, the mean size was 89.4 mm SL (s.d. = 4.0, N = 45). The mean breeding sizes of these three groups are significantly different (ANOVA, F = 154, p <0.001).

Nest occupancy by males: Ninety percent of the nests were occupied between 0600-1200 h (Fig. 3). An occupied nest was defined as one where the male was attacking other fish or building up the nest. Occupancy estimates, therefore, are under­ estimates, as males occasionally wandered away from their nests. All except perhaps the very smallest nests were defended between 0600­ 1100 h. The males left for deeper water between Depth (m) 1100-1400 h. Departure time varied on different days. Breeding males were seen feeding on zoo- Fig. 2. Depth distribution of C. eucinostomus based on 100 m 2 transects, 0-5 m above substrate. Line equals one standard error plankton while my coworkers and I were diving on either side of the mean. N = Number of 100 m2 transects. between 10-25 m. At 1500 h, 90% of the nests were unoccupied, though a few males were still seen 73.8 cm (N = 15; s.d. = 12.8); top diameter 28.0 cm defending nests. At 1630 h, males began to return (s.d. = 5.4); and height 15.2 cm (s.d. = 3.8). At and 75% of the nests were occupied at dusk. During Nkhata Bay, dimensions were: base diameter 54.2 the night, both males and females rested on the cm (N = 15, s.d. = 9.7); top diameter 24.8 cm bottom with all their fins spread. It was not possible (s.d. = 3.1) and height 8.2 cm (s.d. = 3.1). The to determine, at night, which males were associated Cape Maclear nests were significantly wider at the with a nest. At dawn, however, all nests were base (Mann Whitney U, p<0.01) and taller (Mann occupied. Whitney U, p<0.01), than the Nkhata Bay nests, but there was no significant difference between the diameters of the top of nests from Nkhata Bay and £. eucinostomus Cape Maclear.

Deeper arena: An isolated arena, with approxi­ mately 40 nests was observed during July 1979, A ugust 1980, and February 1981 on a m arked site 21 m deep off the main research site. The estimated spacing between nests was 1.5 m. No other C. eucinostomus nests have been observed below 14 m along the sandy beach. Nevertheless, on the west side of W. Thumbe Island, C. eucinostomus arenas have been observed in narrow sand chutes going from 5 m down to 30 m.

Sizes of breeding males: On the large breeding Time arena, the mean size of the males was 95.3 mm SL Fig. 3. Proportion of male C. eucinostomus on nests throughout (s.d. = 3.6, N = 16) during January 1978 and was the day. Number above each bar equals nests observed during 108.0 mm SL (s.d. = 5.8, N = 41) during July, that hour.

85 Table 1. Percentage of nests occupied by male Cyrtocara eucino­ Behavior o f males on arena: In general, males were stomus with and without cormorants fishing. more active in the morning than those few which remained on the arena in the afternoon. In the No cormorants With cormorants morning males courted females three times as much

H 0700 0800 0900 0700 0800 0900 as during the afternoon (Fig. 4, Mann Whitney U, N 219 104 205 110 62 64 p<0.01) and more time was spent building sand % 83.6 88.5 82.9 3.0 0.0 9.4 nests. The morning average of moving one mouth­ ful of sand onto the nest every 15 seconds was approximately four times greater per male than in Cormorant fishing: When cormorants were present the afternoon (Fig. 4, Mann Whitney U, p<0.01). most fish fled to deeper water and most nests were Furthermore, a greater number of aggressive inter­ briefly unoccupied (Table 1). The cormorants actions occurred in the morning. Conspecifics were dived for an average of 45 seconds (s.d. = 10.5, threatened and attacked at an average of 5 times per N = 40) and did most of their hunting above 10 m. 15 min in the morning and 3.1 times per 15 min in While SCUBA diving I have occasionally seen the afternoon. The average number of threats and cormorants at 15 m. Based on observations from attacks on heterospecific fish was approximately 16 the beach, they seldom dived in water deeper than 18 m. During June and July 1979 flocks of 500­

1,000 cormorants flew to the arena from a nesting 20 - 1 10600-1258 tl 20 colony at Mumbo Island, approximately 8 km IH1300-1SOO h away. They fished (between 0545-0700 h) for 20-60 KI5 min. After fishing 5-10 min in one area, the entire f 15 E u> flock would fly 500 m down the beach and begin fishing again. After they left the area the nests were 10- -10 I f t all reoccupied within 15 min. Fishing as a flock, however, was unusual. Cormorants commonly fish­ * 5- -5 ed either alone or in groups of 4-6, in the morning. No flocks of cormorants were on the arena during I k JJ i these same m onths in 1980. Conspecifics Heterotp«cifics

Tagging of males: Forty percent of the 120 tagged males immediately returned and defended the nest from which they were taken. The other 60% either fled, or had lost their nest to another male while being tagged. In all cases where a male was removed from the nest and did not return, another male took over the nest within 5 min. No individually recog­ nizable or tagged male was ever observed on the same nest the following day. In fact, only one tagged male was ever observed on a nest the following day and that particular male was ob­ Move Sand served 30 m down the beach on another nest. Ten percent of the tagged males were later seen moving Fig. 4. Morning and afternoon behavior of males on nests per over the arena in breeding color, but not actively 15 min watch per male. Height of bar equals the mean and lines defending a nest at the time of sighting. are one standard error on either side of the mean. All inter­ actions, except the attacks on conspecifics, were significantly different between morning (N = 34) and afternoon (N = 9) (Mann Whitney U, p<0.01).

86 per 15 min in the morning and one-half that figure in the afternoon (Mann Whitney U, p<0.01). Conversely, feeding activity was greater in the afternoon. At this time the few males remaining on the arena foraged on zooplankton above the nest at a rate 10 times higher than in the morning. A major change in behavior from morning to afternoon was the switch from moving sand to foraging and most males left the arena. The male courtship display consisted of sharp up and down zig-zag motions in the water column. If attracted by the male, a female entered the nest and began circling with the male. The shortest recorded time from entry into the nest to the first egg being laid was 15 sec. While a female was in the nest, the male had to break off circling 90% (N = 61) of the time to attack other males in breeding color or C. eucinostomus in non-breeding color (65-80 mm SL). These fish entered the nest at a time when the female was circling and about to lay eggs. They then attempted to circle with her. This occurred most often when the resident male was temporarily away chasing another fish. The non-breeding colored fish observed circling were the same size and color as the breeding females, but I suspect that they were males. Of fish chased into gill-nets by SCUBA divers during April and October 1978, 39 were males between 66-85 mm SL. Thirty-two were ripe and capable of producing sperm. All had the non-breeding silvery coloration. Their mean SL was 71.7 mm (s.d. = 3.8 mm). This was the size range of breeding females on the arena (Fig. 5) as well as the individuals invading the nests and attempting to circle with ripe females. Conspecifics also entered the nest to cannibalize eggs, and males on the nest were observed to swim around after the female had laid her eggs and to eat them. Of 301 eggs observed laid in nests five percent were cannibalized by the territorial males and two percent were eaten by other conspecifics. Standard length mm

Female behavior: The females (N = 25) I followed Fig. 5. Number of eggs in the gonads of C. eucinostomus versus laid all of their eggs (35-57) on a maximum of 4-12 standard length (mm). When the eggs were between 0.1-1.4 mm nests. They often visited the same male more than and 1.5-3.0 mm in diameter, there were no correlations between number of eggs and the size of the fish. For eggs greater than once, a behavior also observed in C. argyrosoma 3.0 mm, there was a significant correlation of great number (personal observation). However, due to the wide of eggs for a larger fish (r = 0.49, p<0.01; # eggs = ranging habits of females and the lack of sufficient -103.8 + 1.99 (SL)).

87 markers on the arena, it was not always possible to water column was relatively rare on this arena, but determine if a male being visited had previously it was common on other arenas (personal observa­ fertilized her eggs. Females laid between 1-6 eggs tion). Most attempts at egg eating on this arena during each circle and if undisturbed, laid up to 20 were from conspecifics entering from the side. eggs with a single male, But usually they were only able to lay eggs during one or two circles before Feeding behavior: Cyrtocara eucinostomus fed prim ­ they were interfered with by other fish entering the arily upon two groups of zooplankton, Diaphano- nest. Females moved along the shoreline laying soma and diaptomids (Table 3). In all collections of eggs for distances of at least 100 m and, I suspect C. eucinostomus from various areas throughout the further. The females I observed laid all their eggs Cape Maclear region, over 90% and sometimes as within 60 min. much as 99% of the diet consisted of these two genera. The four collections made between 5-15 m Egg number and size: Eggs have a diameter of on the breeding arena indicated that fishes on the between 3.0 and 3.5 mm when laid. There is a arena also fed upon these two genera. They took correlation between the number of eggs in the ovary larger size classes of Mesocyclops, Diaphanosoma and the female’s standard length when the largest and the diaptomids than would be predicted if they eggs are 3.0 mm or larger (Fig. 5). But when the captured individual plankters relative to their size- eggs are smaller in the ovaries, there is no such frequency distribution in the water column (Fig. 6). correlation. It appears that females have eggs in various stages of development (Table 2). Three Zooplankton depth distribution and seasonality: For females with embryos in their mouths had small over two years of sampling there was consistently eggs (0.1-1.4 mm) in their gonads. less zooplankton in 5 m of water than in 15 m (fig. Females on this arena were occasionally followed 7). Over the arena, there appeared to be a bimodal by a single Cyrtocara labifer while they were laying peak of Diaphanosoma and/or diaptomids at the eggs. Cyrtocara labifer dived into the nest from 3 m beginning of the rains in December-January and above it as the female released her eggs and before again at the beginning of the mwera or southerly she got them into her mouth. The occurrence of winds, in June-July in 1979 and 1980. In the nine specialized egg eaters attacking from up in the months of sampling in 1980, there were significantly

Table 2. Number of eggs of each distinct size class in the gonads of female C. eucinostomus on July 15, 17, 18, 1980.

SL Total # of eggs

87 36 30 (2.1 mm) 6 (1.1 mm) 80 24 24 (0.7 mm) 60 27 27 (0.5 mm) 75 30 16 (1.1 mm) 9 (0.6 mm) 5 (0.5 mm) 81 38 18 (1.7 mm) 12 (0.8 mm) 8 (0.3 mm) 75 28 10(1.1 mm) 14 (0.5 mm) 4 (0.3 mm) 77 52 26 (1.1 mm) 17 (0.6 mm) 9 (0.5 mm) 90 32 6 (1.3 mm) 8 (0.8 mm) 14 (0.6 mm) 89 40 10 (1.5 mm) 12 (0.6 mm) 18 (0.3 mm) 82 31 12 (1.8 mm) 14 (0.4 mm) 5 (0.3 mm) 79 32 8 (1.0 mm) 18 (0.6 mm) 6 (0.3 mm) 68 30 24 (0.7 mm) 6 (0.6 mm) 77 46 40 (1.0 mm) 6 (0.5 mm) 73 38 24 (0.8 mm) 14 (0.4 mm) 86 52 30 (1.5 mm) 8 (0.6 mm) 14 (0.4 mm) 64 18 16 (3.3 mm) 2 (0.3 mm)

88 Table 3. Mean number of plankters in stomachs of C. eucinostomus collected on arena, standard deviation in parentheses.

Date N Diaptomus Diaphanosoma Mesocyclops Bosmina Chaoborus

2/2/78 38 35.2 29.5 5.9 0.2 0.0 (11.7) (11.7) (2.5) (0.1) (0.0) 2/16/78 44 105.9 221.0 20.9 0.5 0.05 (29.9) (157.9) (6.0) (0.1) (0.02) 4/1/78 18 24.4 28.5 2.0 0.05 0.1 (11.0) (7.2) (0.4) (0.02) (0.05) 4/17/78 25 173.9 7.7 1.3 0.0 0.2 (56.0) (3.0) (0.5) (0.0) (0.1)

more zooplankters than in 1978/79 (Mann Whitney tilapia oxyrhynchus were observed to capture non­ U, p<0.01, Fig. 7). There was also a great deal of breeding C. eucinostomus at the interface of Pota- variation in the clarity of the water. Water was mogeton weed beds and sand. I observed no other clearest in September-November but again yearly species capturing C. eucinostomus. variation was great (Fig. 7).

Temperature: The surface water temperature reach­ ed a peak of 29.5° C in January - March and dropped to a low of 22° C in July and August (Fig. 8). The difference between the surface and 10 m was usually less than 0.5° C and never m ore than 1.5° C.

Diurnal fish predation: Schools of Cyrtocara ki- winge occasionally appeared at dusk above the arena. They captured both male and female C. eucinostomus along with other fishes. Most of the potential prey swam to deeper water, such as they did when cormorants appeared. Three times Hemi-

Maaocvcloos Diaphanosoma Diaptom ids

• 0 .4-

% 0.2-1

0.6 0.8 1.0 1.2 1.4 1.6 02 0.4 0.6 0.6 0.6 0 6 1.0 1.2 1.4 1.6 S I Z E (mm)

Fig. 6. The frequencies of larger size classes of Mesocyclops Fig. 7. A. Secchi disk reading at main study site. Line above and spp. (y1 = 44.5, d.f. = 5, p<0.01), Diaphanosoma (/2 = 22.4, below mean equals one standard error. ‘N’ on bottom of graph d.f. = 5, p<0.01), and diaptomids ( j 2 - 60.7, d.f. = 5, p<0.01) equals number of measures on different days during 3-month in the stomachs of C. eucinostomus are significantly greater than period. B. Density of zooplankton that C. eucinostomus feeds on the expected frequencies based on simultaneous water samples. at 5 m and 15 m.

89 N D J F M A M J JASON DJ FMAMJ JASONDJF

1978 1979 1980

Fig. 8. Seasonal water temperature fluctuations in the Cape Maclear region.

Nocturnal predation on arena and comparison of catfish catch between nets at 9 m and 21 m: Catfish were commonly seen on the arena at night and fled when lights were shone on them. In 349 catfish caught in the trammel nets, 65% of the stomachs were empty. Seventy-three stomachs had cichlid remains that could not be conclusively identified to species. Of these remains 95% could have been C. eucinostomus. Of the 47 stomachs where the con­ tents could be conclusively identified to species 37 contained C. eucinostomus. There were a total of 63 individual C. eucinostomus in these stomachs. On ten of the eleven nights on which the paired nets were set, the deeper net at 21 m caught more catfish than that at 9 m (Wilcoxon, p <0.01). The net set on the arena between 7-10 m caught a mean of 1.5 catfish (s.d. = 0.7). Nets set between 20-25 m caught a mean of 3.7 catfish (s.d. = 1.4). Catfish i — i i i ■ i i were never observed by day. 10 20 30 40 50 60

Middle depth Im ) of the net Depth distribution of catfish: The 180 m trammel nets set throughout the Cape Maclear region at Fig. 9. Number of Bagrus meridionalis caught in trammel nets versus the depth of the net. There is a significant correlation of depths down to 60 m caught significantly more the number of catfish caught and increasing depth. (Bagrus fish in deeper than in shallow water (Fig. 9). meridionalis caught per 180 m net = 1.57 + 0.31 (depth (m)), r = 0.49, p<0.05).

90 Discussion not so brilliantly colored and are often drab. Many Sarotherodon species fit this pattern (Lowe 1956a) General characteristics of arena behavior and breeding C. eucinostomus are sexually di­ morphic. The territorial males are larger than the The reproductive system of the maternal mouth­ females and are bright blue with their anal and brooding cichlids is analogous to bird leks (Fryer caudal fins edged with a yellow and black border & lies 1972). The existence of cichlid arenas has (Fig. 1), while the females are a rather non-descript been well documented for the Sarotherodon, silvery gray. where many of the species have a lekking mating system (Ricardo-Bertram 1943, Lowe 1953, Lowe- 4) Sneaky males: In some species of birds, such as M cConnell 1956a, b, 1957, 1958, 1959, Fryer 1961, the prairie chicken, there are males which mimic Fryer & lies 1972). Other genera of cichlids also females in order to gain entrance to the lek. Once in engage in lekking behavior (Kirchshofer 1953, the lek they will try to court females and unless Fryer & lies 1972), but they have been less well chased out by the resident males, may sneak a studied. The mating system of C. eucinostomus is successful fertilization (Wiley 1974). This phenom­ similar to the classical avian leks. Characteristics it enon of ‘sneaky’ males also appears to be common shares with bird leks are: in fish (Warner et al. 1975, Gross 1979, 1980, Gross & Charnov 1980). In the case of C. eucinostomus, 1) No male parental role: Most ornithologists the ‘sneaky' males remain silvery, like the females, (Armstrong 1947, Lack 1968) and sociobiologists and are the same size as the females. They swim into (Wilson 1975, Barash 1977) define a ‘true’ lek as the nest and fertilize the eggs or else eat them. being removed from the area where the young are Resident males direct many of their attacks at these raised. Males play no role in the care of the young, smaller males which look identical to females. as is true for C. eucinostomus males. Shortly after the female lays her eggs, she leaves the arena. The 5) Lek is away from primary feeding grounds: A eggs are incubated in the female’s mouth and the further requirement of a ‘true’ lek is that it be young are not deposited over the lek. removed from the feeding grounds of the species (Wilson 1975). This distinction also holds for C. 2) Absence of monogamous pair bond: A nother eucinostomus. These fish follow the pattern of many characteristic of bird leks is communal displaying birds (Loiselle & Barlow 1979), courting primarily and multiple matings by males. Often a small in the morning and foraging in the afternoon. number of males is responsible for the majority of Similar to many avian leks, leks of C. eucinostomus the fertilizations (Wiley 1973). Ruwet (1963) reports are occupied for only part of the day. These that both males and females of the cichlid species territories are clearly not defended to protect a food Sarotherodon macrochir are polygamous. Such is resource. the case for C. eucinostomus. There is a complete absence of monogamous pair bonding. Like all of 6) Presence of sexually inactive males: In some avian the lekking cichlid species studied so far in Lake leks, sexually inactive males visit the lek site during Malawi (C. argyrosoma, L. furcicaudajfurcifer, C. periods of no reproductive activity (Wiley 1973). nigritaeniatusjpleurotaenia, L. variabilis, L. liturus, Loiselle & Barlow (1979) report that there is no L. aurita (personal observation)), C. eucinostomus is recorded instance of this occurring in fish, but they both polygynous and polyandrous. speculate that such lek visitation does occur. Males with small ‘non-ripe’ testes have been frequently 3) Sexual dimorphism: Birds which lek often exhibit collected on the arena in the afternoon. Whether or a high degree of sexual dimorphism with the males not they are capable of producing sperm is un­ being among the ‘most colorful of the bird world’ known. I suspect, however, that they are among (Wilson 1975). The females, however, are usually those who cannibalize eggs; as they feed, their

91 gonads then develop and they eventually do sneak 10) Mobility: Loiselle & Barlow (1979) state that fertilizations. But it is unclear as to whether or not one of the prerequisites to lekking for any species is such males eventually grow to become territory that individuals must be mobile enough to travel to holders. They may always remain ‘sneakers,’ as has the lek. Cyrtocara eucinostomus is a highly mobile been found to be the case for some centrarchid species, which shoals throughout the lake (Fryer & fishes (Gross 1980, Gross & Chamov 1980). lies 1972). Unlike other more sedentary species which occur over sand, I had no sightings of C. 7) Traditionally: Bird leks are often traditional, eucinostomus which had been tagged for over a reoccurring in the same area every year (Armstrong month. These other species (such as C. moori, 1947, Wilson 1975, Loiselle & Barlow 1979). Lack Kocher & McKaye 1982) do not lek. As in birds, (1968) suggests that lek species might use tradi­ lekking may have evolved to bring together highly tional display sites because they are areas that have dispersed mobile individuals for the purpose of proven to be safe from predators in the past. The 4 breeding. km arena studied here has existed for at least 3 years, and as will be discussed later, probably is a Location of arena site where nocturnal predation is low. Also the smaller deep arena at 21 m was situated in the The location and size of an arena where males gather same location for three successive years. to display are probably influenced by several fac­ tors. Hypotheses to account for the choice of the 8) Synchrony: Clearly for a lek to function year site include its being an area: 1) of abundant food, round, some proportion of the males and females of 2) of suitable substrate, 3) of minimal competition, a species must be reproductively active. In the case 4) where habitat constraints relating to physical of C. eucinostomus, there are always some males factors are low, 5) where visibility of male displays displaying on the large arena and always some to females is high, or 6) of minimal predation females capable of producing eggs. During certain pressure. periods, apparently correlated with high zooplank- ton densities, more males and females move into the 1) Availability of food: Cyrtocara eucinostomus fed arena and it expands. Also, other smaller arenas are almost entirely on zooplankton (Table 3), taking formed, when the proportion of the population larger individuals of the key species (Fig. 6). They breeding increases. also took the cladoceran Diaphanosoma excisum at a smaller size than they did the copeods Tropo- 9) Lack of environmental constraints upon the arena: diaptomus kraepelini, Thermodiaptomus mixtus and Pitelka (in Loiselle & Barlow 1979) claims that it is Mesocyclops spp. (Fig. 6). This preference for necessary to show that there are available, but cladocerans over copepods appears to be a general unused, sites for an aggregation of males to be feature of zooplankton feeding fishes (see Zaret considered a ‘true’ lek. Cyrtocara eucinostomus 1980). At all times zooplankton densities were arenas also fulfill this criterion. The arena expands greater in 15 m of water, just further offshore of the and contracts with the density of males and some C. arena, than on the arena. Males moved off the eucinostomus have been observed breeding down to arena in the afternoon to feed in deeper water. The 30 m deep. There are no known environmental availability of food on the arena was thus unlikely constraints that require the males to be congregated to be the primary factor in the location of the precisely where they are. They are coining together breeding arena. However close proximity to off­ by mutual attraction to breed, and as suggested by shore areas of high plankton density may be im­ Lack (1968) they have congregated in an area where portant. predation risk might be less. 2) Suitable substrate: Cyrtocara eucinostomus were able to breed in areas with fine to coarse sand. They

92 also bred on rocks in areas where they could pick b) Oxygen: In the Cape Maclear region, the lake up sand and build nests on the rock. When the is well mixed. There is no evidence that 0 2 is substrate over the arena was experimentally ma­ limiting above 100 m (Eccles 1974). Thus oxygen is nipulated by building cement reefs, the males built unlikely to be the critical variable in the location of nests on the cement blocks (personal observation). the lek. In some cases, C. eucinostomus were observed c) Waves: There is some evidence to suggest defending a territory and courting females on bare that wave action discouraged C eucinostomus from rock. Areas of suitable sand substrate, but without building nests in shallow water. Fryer & lies (1972) C. eucinostomus, were present in deeper water off report that nests of this species at 4-8 m in Nkhata the arena and in shallow areas throughout the Cape Bay were destroyed by waves during a storm. This Maclear region. Substrate quality appeared un­ destruction of nests due to storms also occurred on likely as the primary determinant of nest location. the Cape Maclear large arena. The shallow nests were, of course, the first to be destroyed. The 3) Competition: There was no evidence that any worst storms occurred during the rainy season, species of fish was aggressively excluding C. eucino­ December-April, and I never saw a nest shallower stomus from any area over sand. There was a than 3 m during this period. However, during July ‘surplus’ of space over the sand. All of the species and August, when the arena was sheltered from the that bred at greater depths, such as C. argyrosoma, prevailing southerly winds, I often saw nests in 1-3 had small arenas, with no more than 50 individuals. m of water. The area where this arena is located is If C. eucinostomus males had attempted to establish probably one of the most protected areas in Lake nests in deeper water, no other territorial fish would Malawi. The islands to the north and east break the have been present to oppose them. Occasionally, waves generated from northern storms. The main­ solitary males with nests were seen, but if they were land blocks the effects of the strong southerly winds not joined by other males, the nests were abandon­ (mwera) that blow during the dry season. ed. No species had nests shallower than C. eucino­ stomus and there was no evidence that any fish 5) Visibility: The hypothesis that males might breed excluded them from the very shallowest waters. in shallow water because it is the best place for Occasionally, C. eucinostomus nests did appear in females to see them was considered. Light intensity water as shallow as 1 m. Thus competition for space is higher in shallow water and male displays might does not appear to be the main factor in the be most pronounced and conspicuous here. How­ location of the breeding area. ever, C. eucinostomus males with nests have been observed down to 35 m in certain sand chutes off 4) Habitat constraints: W. Thumbe Island. Females were seen spawning a) Temperature: Temperature differences be­ with males in nests at 21 m in the two deep arenas. tween depths did not appear to affect their breeding No nests or males were found between 12-21 m. behavior. Cyrtocara eucinostomus bred all year There was no correlation of water clarity (Fig. 7A) round, at temperatures from 29.5° to 22.0° C (Fig. with breeding activity on the arena. In fact, periods 8). The difference between the surface and 10 m was of greatest visibility, September-November, were usually less than 0.5° C and never m ore than 1.5° C. times when fewer nests were present. While this Below 10 m, the change in temperature was even evidence suggests that well-lit, shallow water and less. A thermocline formed during calm periods in enhanced visibility are not essential for successful November-March, but the temperature at 100 m reproduction in this species, further work, involving was still above 24° C (Makwinje, personal com­ careful experimentation is required to test whether munication). One of the peaks of breeding took these factors are important in determining relative place during the coldest time of the year; con­ reproductive success of males. Given the poor sequently temperature seems an unlikely explana­ visibility that cichlids often encounter, such as in tion for the observed pattern. Lake Victoria (Greenwood 1974) or the Lakes of

93 Nicaragua (Barlow 1976, Baylis 1974, McKaye & Other characteristics of C. eucinostomus breeding Barlow 1976), it seems likely that bright, clear water behavior is not crucially important to successful courtship in this family. Time on arena: The amount of time the males can spend on the arena is probably limited by how 6) Predation: Wave action and cormorant preda­ much energy they can acquire. The best data tion probably kept the males from breeding at high available on how long males breed are for C. densities between 0-3 m. Were they to breed below eucinostomus in a nearby small polyspecific arena 12 m, bird predation would decrease, but predation and for C. argyrosoma (McKaye, in preparation). by nocturnal predators, such as clariid and bagrid The data suggest that for these situations, males catfish would be much higher. Catfish were already remain on the arena for two weeks. In all likelihood known to be important predators of cichlid fishes individual males were continually moving off and on (Fryer & lies 1972). This study confirms earlier the large arena. Approximately 5% of the eggs are work which reported that Bagrus meridionalis cannibalized by males. The energy from these fed heavily upon Cyrtocara of the utaka group potential offspring may allow a male to stay on the (Jackson et al. 1963, Eccles et al. 1965). arena longer and perhaps, in the long run, fertilize Over twice as many catfish were netted at 21 m more eggs. It would be interesting to know what the than at the edge of the arena (9 m). Furthermore, optimal amount of cannibalization is to maximize sampling down to at least 50 m throughout the offspring by the male and what a female can do to Cape Maclear region indicates that there is a minimize predation on her eggs by males. Because significant increase in Bagrus with increasing depth of the presence of eggs of a wide range of size classes (Fig. 9). No catfish were ever seen during the day within the gonads of a single individual, as well as between the mainland and W. Thumbe Island (max. the presence of eggs in the females with young in depth observed 32 m) yet they appeared on the their mouths, I suspect that females have 2-4 arena at night and were caught in nets that were set broods per year. overnight. Cichlids in the Cape Maclear region ‘sleep’ with Nest size and shape: Much of a male’s activity in the all their fins spread. This tonic erection of sharp morning was devoted to the building up of the spines makes them appear larger and more difficult height of his nest. Males with the tallest nests got for a predator to handle. At night, the arena was more fertilizations, and these nests were more literally covered with sleeping cichlids. C. eucino­ vigorously defended (McKaye & Louda 1982). The stomus could, of course, avoid catfish predation by nests are designed such that the eggs roll to the remaining up in the water column, by adjusting center where it is less likely that ‘sneaky’ males will their swim bladders for neutral buoyancy. But given move in or that fishes on the substrate will be able the currents in the area, they could be swept away as to come in from the side and eat them. The nest much as 10-15 km in a night. It is, therefore, however provides no protection from egg eaters advantageous to stay put on the bottom. that are attacking from up in the water column, It appears that nocturnal predation is responsible such as C. labifer, C. ovatus and C. insignis. for the crowding of this large stock of fish into shallow waters. The bulk of the courting, therefore, Geographical variation: There is much variation in occurred in the morning while all the fish were in the form of the arenas and the behavior of the males place. When most of the females capable of breed­ in different areas of the lake (lies, personal com­ ing that day finished laying their eggs, the males munication). At Nkhata Bay, the size of breeding moved to deeper water to feed. They returned in the C. eucinostomus males was less than that of those evening and the cycle repeated itself. breeding at Cape Maclear at the same time. Their nests were smaller and extended down to 18 m. The arena was much smaller, with approximately 100

94 individuals, and the males were on the arena in the Barash, D.P. 1977. Sociobiology and behavior. Elsevier, New afternoon. Further comparative work is warranted. York. 378 pp. Also, differences in behavior between different Barlow, G.W. 1974. Contrasts in social behavior between Central American cichlid fishes and coral-reef surgeon fishes. groups of C. eucinostomus males in a polyspecific Amer. Zool. 14: 9-34. breeding arena and the main study area are dra­ Barlow, G.W. 1976. The Midas cichlid in Nicaragua, pp. matic. On the polyspecific arena, tagged males 333-358. In: T.B. Thorson (ed.) Investigations of the Ichthyo- stayed on nests for up to two weeks and all stayed fauna of Nicaragua Lakes, Univ. Nebraska, Lincoln. on the nest in the afternoon, even though courtship Baylis, J.R. 1974. The behavior and ecology of Herotilapia multispinosa (Teleostei, Cichlidae), Z. Tierpsychol. 34: 115-146. activity was low (McKaye, in preparation). On this Beuchner, H.K. 1961. Territorial behavior in the Uganda Kob. polyspecific arena, space appeared to be limited. Science 133: 698-699. Wherever I have observed C. eucinostomus breed­ Brichard, P. 1975. Reflexions sur le choix de la nidification ou de ing, the form of the nest has been the same, though l’inverbation buccale comme mode de reproduction chez there are great differences in its height. Courtship certaines populations de poissons Cichlides du lac Tanganyika. Rev. Zool. Bot. Afr. 89: 871-888. patterns appear to be the same and the laying of Crook, J.H. 1965. The adaptive significance of avian social eggs primarily in the morning appears to be con­ organization, pp. 181-218. In: P.E. Ellis (ed.) Social Organi­ sistent. But the time on the nest, the height of the zation of Communities, Symp. Zool. Soc. London 14. nest, the size of the arena, depth of the arena and Eccles, D.H. 1974. An outline of the physical limnology of Lake diurnal patterns of activity all vary locally, in Malawi (Lake Nyasa). Limnol. Oceanogr. 19: 730-742. Eccles, D.H., R.B. Williamson & R.G. Kirk. 1965. Annual response to a variety of ecological conditions. report for the year 1963/64. Fisheries Research (Part 2). Govt. Further comparative and experimental studies are Printer. Zomba. required before a general synthetic theory explain­ Fryer, G. 1961. Observations on the of the cichlid fish ing cichlid lekking behavior can be achieved. Tilapia variabilis (Boulenger) in the northern waters of Lake Victoria (East Africa). Rev. Zool. Bot. Afr. 64: 1-33. Fryer, G. & T.D. lies. 1972. The cichlid fishes of the Great Lakes of Africa. Oliver and Boyd, Edinburg. 611 pp. Acknowledgements Greenwood, P.H. 1974. The cichlid fishes of Lake Victoria, East Africa: the biology and evolution of a species flock. Bull. Br. I thank T. Kocher, R. Makwinja, W. Menyani, O. Mus. Nat. Hist. (Zool.) Suppl. 6: 1-134. Mhone, M. Oliver and S. Twombly for help in Gross, M. 1979. Cuckoldry in sunfishes (Lepomis: Centrarchi- dae). Can. J. Zool. 57:. 1507-1509. collecting the data presented here. G. Barlow, L. Gross, M. 1980. Sexual selection and the evolution of repro­ Buss, G. Fryer, T. Kocher, P. Loiselle, S. Louda, C. ductive strategies in sunfishes (Lepomis: Centrarchidae). Mackenzie, R. Lowe-McConnell, M. Oliver, P. Ph.D. Thesis, University of Utah. 319 pp. Reinthal, T. Sullivan and S. Twombly and an Gross, M. & E. Charnov. 1980. Alternative male life histories in anonymous reviewer made useful suggestions and bluegill sunfish. Proc. Nat. Acad. Sci. 77: 6937-6940. Jackson, P.B.N., T.D. lies, D. Harding & G. Fryer. 1963. Report criticisms of the manuscript. The cooperation of on the survey of northern Lake Nyasa, 1954-55. Govt. the Malawi Government is greatly appreciated. Printer, Zomba. Financial support was provided by the Smithsonian Keenleyside, M.H.A. 1979. Diversity and adaptation in fish Oceanographic Sorting Center, the World Wildlife behaviour. Springer-Verlag, New York. 208 pp. Fund, and NSF Grant DEB 79-12338. Kirchshofer, R. 1953. Aktionssystem des MaulbrUters Haplo- chromis desfontainesii. Z. Tierpsychol. 10: 297-318. Kocher, T. & K.R. McKaye. 1982. Territorial defense of heterospecific cichlids by Cyrtocara moori in Lake Malawi References cited Africa. Copeia. (In press). Lack, D. 1968. Ecological adaptations for breeding in birds. Armstrong, E.A. 1947. Bird display and behaviour. Lindsay Methuen, London. 409 pp. Drummond, London. 431 pp. Loiselle, P.V. & G.W. Barlow. 1979. Do fishes lek like birds? pp 31-75. In: E. Reese & FJ. Lighton (ed.) Contrasts in Balon, E.K. 1977. Early ontogeny of Labeotropheus Ahl, 1927 Behavior: Adaptations in the Aquatic and Terrestrial En­ (mbuna, Cichlidae, Lake Malawi), with a discussion on advanced protective styles in fish reproduction and develop­ vironment, John Wiley & Sons, New York. Lowe, R.H. 1953. Notes on the ecology and evolution of Nyasa ment. Env. Biol. Fish. 2: 147-176.

95 fishes of the genus Tilapia, with a description of T. saka tions of the Ichthyofauna of Nicaraguan Lakes, University (Lowe). Proc. Zool. Soc. Lond. 122: 1035-1041. Nebraska, Lincoln. Lowe-McConnell, R.H. 1956a. Observations on the biology of McKaye, K.R. & S.M. Louda. 1982. Experimental removal of Tilapia (Pisces: Cichlidae) in Lake Victoria, East Africa. E. nests of a lekking cichlid fish in Lake Malawi, Africa, Afr. Fresh. Fish Res. Org. Suppl. Publ. 1: 1-72. (manuscript). Lowe-McConnell, R.H. 1956b. The breeding behaviour of Richardo-Bertram, D.K. 1943. The fishes of the Banweulu Tilapia species (Pisces: Cichlidae) in natural waters: observa­ region. J. Linn. Soc. 41: 183-217. tions on T. karomo (Poll) and T. variabilis (Boulenger). Ruwet, J.C. 1963. Observations sur le comportement sexuel de Behaviour 9: 140-163. Tilapia macrochir Blgr. (Pisces: Cichlidae) au lac de retenue de Lowe-McConnell, R.H. 1957. Observations on the diagnosis and la Lufira (Katanga). Behaviour 20: 242-250. biology of Tilapia leucosticta (Trewavas) in East Africa Selander, R.K. 1972. Sexual selection and dimorphism in birds, (Pisces: Cichlidae). Revue Zool, Bot. Afr. 55: 353-373. pp. 87-104. In: B. Campbell (ed.) Sexual Selection and the Lowe-McConnell, R.H. 1958. Observations on the biology of Descent of Man, Aldine, Chicago. Tilapia nilotica (Linne) (Pisces: Cichlidae) in East African Snow, D.W. 1963. The evolution of manakin display. Proc. 13th Waters. Rev. Zool. Bot. Afr. 57: 129-170. Int. Omithol. Congr.: 553-561. Lowe-McConnell, R.H. 1959. Breeding behaviour patterns and W arner, R.R., D.R. Robertson & E.H. Leigh, Jr. 1975. Sex ecological differences between Tilapia species and their sig­ change and sexual selection. Science 190: 633-638. nificance for evolution within the genus Tilapia (Pisces: Wiley, R.H. 1973. Territoriality and non-random mating in sage Cichlidae). Proc. Zool. Soc. Lond. 132: 1-30. grouse, Centrocercus urophasianus. Anim. Behav. Monogr. 6: Lowe-McConnell, R.H. 1969. The cichlid fishes of Guyana, S. 85-169. America, with notes on their ecology and breeding behaviour. Wiley, R.H. 1974. Evolution of social organization and life Zool. J. Linn. Soc. 48: 255-302. history patterns among grouse. Q. Rev. Biol. 49: 201-227. McKaye, K.R. 1977. Competition for breeding sites between the Wilson, E.O. 1975. Sociobiology. The New Synthesis. Belknap, cichlid fishes of Lake Jiloa, Nicaragua. Ecology 58: 291-302. Cambridge. 697pp. McKaye, K.R. 1981. Field observation on death feigning: a Witte, F. 1981. Initial results of the ecological survey of the unique hunting behavior by the predatory cichlid, Haplo- cichlid fishes from the Mwanza Gulf of Lake chromis livingstoni. Env. Biol. Fish. 6: 361-365. Victoria (Tanzania): breeding patterns, trophic and species McKaye, K.R. & G.W. Barlow. 1976. Competition between distributions. Neth. Jour. Zool. 31: 175-202. color morphs of the Midas cichlid, Cichlasoma citrinellum, Zaret, T.M. 1980. Predation and freshwater communities. Yale in Lake Jiloa. pp. 465-474. In: T.B. Thorson (ed.) Investiga­ University Press, New Haven. 187 pp.

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