BEHAVIORAL BIOLOGY, 13,197-202 (1975), Abstract No. 4223

Behavioral Individuality in the Cichlid Fish, Tilapia mossambica

DAVID P. BARASH

Departments of Psychology and Zoology, Univeristy of Washington, Seattle, Washington 98195

Behavioral individuality with regard to courtship and aggression was evaluated and demonstrated among males of the Cichlid fish, Tilapia mossambica. Individuals fall into natural categories within which behavioral differences are not apparent, suggesting a behavioral polymorphism. These categories appear to represent heritable discontinuities; possible ways in which these polymorphisms are maintained are discussed.

Students of animal behavior are beginning to recognize the existence and significance of individual differences in behavior (Hirsch, 1963, 1967). Yet there have been few attempts to evaluate the degree of behavioral individ- uni ty normally present in a population of any species, and those behavioral traits analyzed have usually been the most convenient, rather than the most biologically important. In addition, the genetic basis o f aggressive and sexual behavior is in great need of study. This paper describes behavioral individ- uality in a small sample of male Tilapia mossambica (family: Cichlidae), suggests a genetic basis for the observed individual differences and provides hypotheses as to the factors responsible for the maintenance of the observed heterogeneity.

METHODS AND RESULTS

The initial subjects were seven male Tilapia mossambica, each derived from a different source, including university, institutional and commercial stock. The size o f Tilapia is known to influence its behavior, particularly its aggressiveness (Neff, 1964); therefore, the subjects selected were all of comparable size, ranging from 8.8-9.2 cm (total length). Their ages were not known. Each subject was kept visually isolated in a 5-gal tank for 30 days before testing began. The tests involved successive introduction of each of 2 wooden models, 9.0 cm long, one painted to represent a female T. mos- sambica and the other a male in "Dark II" coloration (Neil, 1964). The order

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TABLE 1

Median Scores for Behavioral Tests of the Seven Original Subjects and their Offspring a

Behaviors

Number of Seconds in Seconds in Latency frontal lateral Number Dark I1 (sec) for displays display of nips or Black initial tilt

Subjects (a) (b) (c) (d) (e)

1 3 133.5 6.5 40.5 74 la 2 140 5.5 20.5 80 lb 3 128.5 6 33 60.5 lc 2 171 7 56 44.5 ld 2.5 134.5 7.5 20.5 101.5 le 1.5 159.5 6.5 37 104

2 2.5 160 7 120.5 60 2a 2.5 170.5 7 96.5 70 2b 2 123 6.5 110 65.5 2c 2.5 134 5 133.5 42 2d 2 160.5 6.5 102.5 31.5 2e 2.5 151 6.5 109 33.5

3 2.5 142.5 5 94 51.5 3a 2.5 155,5 5.5 80 64.5 3b 2.5 103 4 90.5 38.5 3c 3 127 6 122 29 3d 2 128.5 7 123.5 42 3e 3 1 4 4 5 86 36

4 1 83 2 286 15 4a 1.5 74.5 2 285.5 22.5 4b 1 79.5 2.5 284.5 19 4c 0.5 89 1.5 277 6.5 4d 1 97 2 294.5 8.5 4e 1 62.5 3.5 300 20

5 1.5 64,5 1 294 17 5a 1.5 54 2 291 20.5 5b 1.5 50.5 2.5 290.5 12 5c 2 77.5 1.5 274 14.5 5d 1 79 1 281.5 6 5e 1.5 89 1.5 293.5 7.5

6 0 0 0 22 93.5 6a 0 0 0 18.5 110.5 6b 0.5 0 0 34 44 6c 0 20 0 39.5 66.5 6d 0 15 0 42.5 70 6e 0 0 0 20.5 83

7 0 0 0 66 110 7a 0 17.5 0 45.5 94.5 7b 0 0 0 21.5 83.5 7c 0 0 0 57 21.5 7d 0 0 0 58.5 78.5 7e 0 0 0 48 91.5

aUnlet tered numbers indicate sires, subscript letters indicate offspring; each datum represents 30 5-min tests for each individual.

INDIVIDUALITY IN FISH 199

of presentation of the two models was randomly determined each day for each subject. Each model was introduced for a 5-rain test period on each of 30 days during which time aggressive responses (male model) and courtship responses (female model) were recorded as follows: aggressive-(a)frequency of frontal displays, (b)number of seconds (out of a possible 300) spent in lateral display and @)number of nip sequences directed at the model; courtship-(d) number of seconds (out of a possible 300) spent in either "dark II or "black" coloration and (e) latency in seconds between introduction of the model and the initial appearance of "Tilting" behavior. Details of these behavior and color patterns have already been carefully described (Baerends and Baerends van Roon, 1950; Nell, 1964). High scores for a, b and c indicate high aggression; high scores for d and low scores for e indicate strong courtship.

The data (Table 1) were analyzed using a series of Kolmogorov-Smirnov two-sample tests (Siegel, 1956; a non-parametric test was selected because the assumption of normality does not appear to be justified). Two-tailed tests revealed that males 1, 2 and 3 are statistically indistinguishable with regard to behaviors a, b, and c. The same applied to males 4 and 5, and males 6 and 7. The seven subjects thus distributed themselves into three distinct categories of aggressive behavior, within which no individual differences were discernible. However, comparisons of data between individuals of the three categories (d 1 vs d4, d2 vs d7 , etc.) revealed significant differences in all cases (P <0 .0 5 that the data from any two such individuals are drawn from the same statistical population), excepting a lower distinctiveness for behavior A (P<0 . 10 for males 5 or 5 vs males 6 or 7).

The data for courtship intensity (behaviors d and e), revealed a similar pattern of three rather discontinuous categories with similarity among individ- uals within the categories and distinctness between individuals from different categories. However, there was no correlation between individual tendencies for aggressiveness and for courtship intensity, since males 4 and 5 (interme- diate in aggressiveness) were the maximum courters. The other 2 groups consisted of males 1, 6 and 7, and males 2 and 3. Individuals within these courtship groups were statistically equivalent with regard to behaviors d and e. Similarly, the differences between category members was significant (P < 0.05) in all cases.

Having ascertained a degree of behavioral individuality, I attempte d to evaluate the heritability of these differences by obtaining and testing Fl'S. As with the males, the females represented a variety of genetic backgrounds. I randomly selected five male offspring of each subject and isolated them in 7-gal aquaria at 100 days of age. After 30 days isolation these Fl ' s were tested for aggression and courtship intensity, exactly as their sires had been previously.

200 DAVID P. BARASH

The results are included in Table 1. Considering the results for each behavior separately, I tested the hypothesis that the six scores in each case (sire plus five offspring) had been drawn from the same continuous popula- tion, using the Kruskal-WaUis one-way analysis of variance, corrected for ties (Siegel, 1956; because of the data's high variance, determination of formal heritabilities were not feasible). The null hypothesis could not be rejected, at any confidence level. Once again, as with the sires, Kolmogorov-Smirnov tests revealed significant differences (P<0.05) between offspring of different aggression or courtship groups.

DISCUSSION

The above evidence for behavioral individuality, for discontinuous groupings of individuals of similar behavioral tendencies, and for some degree of heritable influence, all suggest (but do not require) the occurrence of behavioral polymorphism among male Titapia mossambica. The occurrence of any polymorphism advertises a situation of considerable evolutionary interest, and this case is no exception. Males showing a high degree of aggression and/or courtship might be expected to experience greater reproductive success; this necessitates some explanation for the apparent persistence of the "lower" category individuals. The phenotypic homogeneity among the offspring of each subject precludes explanations in terms of heterozygosis. An alternative hypothesis is that high levels of aggression and courtship are not as advanta- geous as they may intuitively appear. Some circumstantial evidence supports this notion.

Immediately prior to spawning, male and female circle the nest while both partners engage in fin vibrations and mutual nipping. In addition, the male may briefly leave the nest to chase away other intruding fish. Breeding occurred in 10-gal tanks that were not. in visual isolation from their neighbors, and the males frequently interrupted their prespawning behavior to "chase" the image of a fish in an adjacent tank. Subjects 1, 2 and 3 (the three most aggressive males) averaged 3.4 such chases per min (34 min total), as compared to 1.8 chases/min.for the minimally aggressive males 6 and 7 (22 rain total). The chase frequency for the former males is significantly higher (t-test, P < 0.05). Although the aggressive males did not appear to be reproductively handicapped by their aggressiveness, similar interruptions may be more serious among free-living animals where neighbors are not isolated by glass walls, and lengthy agonistic interactions could ensue, during which the female may be liable to leave the nest. Thus, a phenomenon analogous to "aggressive neglect" already described for birds (Ripley, 1961), may create compensating dis- advantages to highly aggressive males. The immediate advantage of aggressive- ness may accordingly vary with local population density, thereby creating a behavioral polymorphism in the species as a whole.

INDIVIDUALITY IN FISH 201

Finally, in attempting to breed the original subjects, I had difficulty obtaining successful matings, but was eventually successful after exposing females to different males until a compatible combination was found. Of the 7 females used to obtain the Fl's, 5 subsequently spawned with different males of the same courtship morph (7 attempts)-an equal number of attempted matings with males of a different courtship morph produced only 2 successful spawnings. Evaluation of the courtship and aggression characteristics of these two "mismatched" spawnings would have been most instructive. Unfortunately, they all died because of a heater malfunction. It is hoped that further studies will elucidate the female genetic contribution to the behaviors here described.

The above results might suggest a parallel polymorphism among females, with individual differences in the characteristics of preferred male courtship. The exact functioning of these differences is currently being investigated, with the possibility that some females may be induced to flee by excessive speed, or frequency of the following male behaviors: (1)the rapid approach and "tilt" at a female in mid-water, (2)tailwagging during later courtship and (3) forceful nudging of the female immediately following the initial spawning attempts. Thus, d 6 averaged 0.3 tailwags/min during the first 4 min after introduction of a female, whereas d 4 averaged 2.2. Of 93 observed tailwags, 88% were followed by female retreat. If some females are liable to be chased off by males showing high levels of these behaviors but are susceptible to low4ntensity courtship, whereas others are unlikely to be sufficiently stimu- lated by low-intensity courtship, polymorphism in male courtship could be maintained by a complimentary polymorphism in female responsiveness. The situation of non-interbreeding behavioral morphs would be analogous to that of "gentes" suggested for the European Cuckoo (Southern, 1954). Alter- natively, behavioral differences have been correlated with chromatic polymor- phism in the Midas cichlid (Cichlosorna citrinellum) (Barlow, 1973), in which the competitive advantage to one morph in mixed populations is not apparent in unmixed groupings. Polymorphism could thus be maintained in either species if the alternative morphs (one with a potential competitive advantage) do not normally mix in nature.

Further confirmation of the behavioral individuality described here and of the schema proposed for its maintenance must await analysis of the situation obtaining among free-living animals in their natural habitat.

REFERENCES

Barlow, G. (1973). Competition between color morphs of the poly-Chromatic midas cichlid Ciehlasorna citrinellum. Science 179, 806-807.

Baerends, G,, and Baerends van Roon, J. (1950). An introduction to the study of the ethology of cichlid fishes. Behav. Suppl. 1, 1-242.

202 DAVID P. BARASH

Hirsch, J (1963). Behavior genetics and individuality understood. Science 142, 1436-1442.

Hirsch, J. (1967). Behavior-genetic analysis. In J. Hirseh (Ed.), "Behavior-genetic anal- ysis." New York: McGraw-Hill.

Neil, E. (1964). An analysis of color changes and social behavior of Tilapia mossambiea. Univ. Calif. Publ. Zool. 75, 1-56.

Ripley, S. (1961). Aggressive neglect as a factor in interspecific competition in bkds. Auk 78, 386-371.

Siegel, S. (1956). Non-parametric Statistics. New York: McGraw-Hill. Southern, H. (1956). Mimicry in cuckoos' eggs. In J. Huxley (Ed.), "Evolution as a

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