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Interrelationships of dominance and territorial behaviour in the pupfish, Cyprinodon variegatus
Behavioural Processes, 2 (1977) 383-391 o Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
333
Short Communication INTERRELATIONSHIPS OF DOMINANCE AND TERRITORIAL BEHAVIOUR IN THE PUPFISH, CYPRINODON VARIEGATUS M. ITZKOWITZ Department
of Zoology,
University
of the West Indies, Kingston
7 (Jamaica)
(Received 4 April 1977; revised 20 October 1977)
ABSTRACT Itzkowitz, M., 1977. Interrelationships of dominance and territorial behaviour in the pupfish, Cyprinodon variegatus. Behav. Processes, 2: 383-391. Under laboratory conditions, Cyprinodon variegatus establishes either a dominance or territorial mating system. In the dominance system, one male usually has complete access to receptive females, while in the territorial system, several males have equal access. Four factors were observed to enhance a subdominant’s ability to establish a territory and improve his reproductive success; increasing the number of conspecific intruders, increasing the available area, the presence of partial barrier, and the presence of a receptive female.
INTRODUCTION
Territorial and dominance systems serve a large variety of functions for a diverse assemblage of animal groups (Carpenter, 1958). The two systems have two basic factors in common: first, both utilize agonistic behaviour to develop and maintain them, second the dominant and the territorial defender each has the highest fitness within its area of movement (see reviews of Brown, 1975; Wilson, 1975). Theoretically, differences arise with territoriality allowing several individuals to co-exist within a unit area with potentially equal fitness, while the dominant has the highest fitness within the same area. However, if both social systems depend on the same behavioural mechanism, why would a dominant allow other individuals to share the area equally (thereby becoming territorial) and thus reduce its own fitness? Ideally, answers to such questions are best uncovered by the manipulation of specific environmental variables to induce a shift from one system to the other. Unfortunately, most studies which do consider the ecological and evolutionary consequences of these systems are performed on species (e.g., birds) that are difficult to manipulate experimentally. Cyprinodon uariegutus La&p&de, the pupfish, could shed some light on the relationships between these two systems as it can develop and maintain either a dominance or territorial system under certain laboratory conditions. This is not unusual for fish as I, (unpublished) and others (e.g., Greenberg, 1947),
384
have observed it in other species (see definitions below). As the pupfish territory appears to function only for mating, many of the other environmental pressures important for other species (e.g., distribution of food, predator protection, predation) were not considered. Here, I consider four factors which I hypothesized to be important in maintaining one or the other system; the number of intruders, the size of the available area, the presence of a partial barrier, and the presence of a receptive female. These variables were selected, as previous studies have indicated that they are influential in modifying territorial and/or dominance behaviour. DEFINITIONS
Within the confines of an aquarium or cage, it is possible to assume that a dominant is actually a territorial defending the entire area. Traditionally, it has been considered as dominance (e.g., Greenberg, 1947; Bovberg, 1956; Boice and Witter, 1969; Frey and Miller, 1972; Phillips, 1974; Figler et al., 1976), as the overt behaviour differs little between individuals confined in a territory, and one where the subordinates stay within the domain of the dominant. In both situations, the dominant can chase others but is rarely attacked, and has greater access to food and/or mates. Here I continue the traditional definition of a dominant as one that can chase any fish within the entire tank. Territoriality exists only if two or more males defend discrete areas within the same tank and each male is dominant only within its area. MATERIALS
AND METHODS
Cyprinodon uariegutus is a small, cyprinodont fish that reaches sexual maturity at 2-3 cm. The adults in this study were uniformly 40-45 mm. The sexes are dichromic, with the males having a blue irredescent dorsal region, black pectoral fins and a black bar at the edge of the caudal fin. The females are light, with large dark grey or black blotches on the sides of the body. The adults were collected from Port Henderson, Jamaica (on the western side of the entrance to Kingston Harbour), from a small shallow pool (diameter 5 m) located directly behind a sandy beach and surrounded by mangrove plants. While the pool appeared to receive water only from high tides and rain, complete drying was never observed. The specimens were gradually acclimated to freshwater over a 24-h period and then transferred to a large stock tank. After approximately 14 days at a 15-h light cycle, the fish were used in the experiments. All experiments were conducted in glass aquaria (120 X 20 X 30 cm) which were marked lengthwise at l-cm intervals. The depth of the water was 15 cm, which corresponded to the depth of natural territories (Itzkowitz, 1974). Six experiments were conducted using the above aquaria. In all instances, the position of either the dominant or territorial male was noted for a lo-min period, during which a continuous record was maintained of the male’s
385
changes in position. Normally the male made between 150 and 250 position changes during the 10 min. For some experiments an opaque glass partition divided the tank in half (“half tanks”), reducing the length to 60 cm. Experiment I. This experiment was designed to observe the influences of male numbers on the formation of a dominance or territorial system. Three densities (2, 5 and 10 males) were randomly placed in the ten half tanks and allowed to acclimate for 24 h. After acclimation the position of the dominant or territorial male was recorded for a lo-min period. After the observation, all experimental animals and those remaining in the stock tanks, were placed in a bucket and randomly redistributed for the next day’s observations. A total of 75 fish were available for the experiments. Experiment II. This experiment considered the influence of females on the formation of a dominance or territorial system. The same procedures were used here as in Experiment I, but with the addition of two resident females in each half tank. Experiment III. I hypothesized that obstructions which interfered with a dominant’s ability to move swiftly across the half tank or view all aspects of it, would influence the establishment of a territorial or dominance system. The partial barrier divided the half tank into two equal sections across the width. It consisted of a mound of sand tapered into a fine edge, and small pieces of black plastic were projected at irregular intervals along the edge. The experimental procedures used here were identical to those followed in Experiment II. Expc:,Lnent IV. I tested the influence of a larger area on the formation of a social system. The opaque dividers were removed allowing complete access to the entire tank (“full tanks”). The procedures used here follow those of Experiment I (i.e. no female residents) but there was an increase in the number of male densities (2, 5, 10 and 20 males). Experiment V. This experiment was similar to Experiment IV except for the presence of two adult females in each full tank. Experiment VI. In the last experiment I considered the influence of nonterritorial intruders on the stability of a boundary separating two territorial males. Five males were simultaneously placed in a half tank. To stimulate territory formation, a partial barrier (see above, Experiment III) was erected, dividing the substratum area in half. After 24 h two territories were formed, leaving the other three males as non-territorial intruders. Removal of the partial barrier did not immediately influence the territories, as they maintained their respective areas for at least several hours, and in most cases, for the rest of the day. The territorial position in relation to a l-cm scale was
386
recorded every 2 set for 10 min. The three intruders were then removed and after a delay of 45 min, the position of the same male was again recorded. The intruders were then replaced and after a delay of 45 min, the position of the male was recorded for a final time. This was replicated with five different groups in five different tanks. RESULTS
Experiment I. In the half tank, increasing the number of competing males did not significantly increase the appearance of territories (chi-square: P > 0.05, Table I).
TABLE
I
Presence of dominance number of replicates) Number
of males
2 5 10
or side-by-side
territories
in half tanks without
N
With territories
With dominance
5 6 6
0 1 2
5 5 4
females
(N =
Experiment II. The addition of receptive females to the half tanks did not significantly increase the appearance of territories (chi-square: P > 0.05, Table II). There was no significant difference between the number of territories formed in Experiments I and II (chi-square: P > 0.05).
TABLE Presence Number 2 5 10
II of dominance*or of males
territories
in half tanks with females
N
With territories
With dominance
6 6 6
0 0 1
6 6 5
(N = number
of replicates)
Experiment III. The addition of a partial barrier to the half tanks significantly increased the total number of territorial situations in this experiment as compared to Experiment II (chi-square: P < 0.05, Table III). However, within this experiment, increasing the number of males did not influence territory formation. At all densities, a maximum of two territories formed, with most utilizing the barrier as the boundary separating the two defended areas.
387
TABLE III Presence of dominance or territories imhalf tanks with a partial barrier; females were present (N = number of replicates) Number of males
N
Territories
Dominance
2 5 10
6 6 6
3 5 4
3 1 2
Experiment IV. Doubling the available area, by removing the opaque partition, produced significantly more territorial situations (excluding the 20-male density) than the non-barrier experiment (I) (chi-square: P < 0.05, Table IV). There were significantly more territories formed at the higher densities (10 and 20) than at the lower densities (2 and 5) (Fisher test: P = 0.01, two tailed).
TABLE IV Full tanks (double area); without females (N = number of replicates) Number of males
N
Territories
Dominance
2 5 10 20
5 6 6 6
0 2 6 6
5 4 0 0
Experiment V. With the addition of females, there was a significant increase (chi-square: P < 0.05) in the number of territories formed at the low densities as compared to Experiment IV (Table V).
TABLE V Full tanks with females Number of males
N
Territories
Dominance
2 5 10 20
6 6 6 6
4 5 6 6
2 1 0 0
388
Experiment, VI. The 300 position points recorded for a male revealed that the boundaries separating the two males had no sharp demarcation. Thus, the outermost limit of a male’s movement often over-lapped with the outermost movement of his neighbour. As there was no sharp boundary line, direct measures of boundary changes were not possible. An alternative procedure used was to calculate the area within which the male confined 80% of his movements. The calculation entailed the number of times the male was observed at a l-cm mark and began at the furthest point from his territorial neighbour. Thus the first l-cm mark was closest to the end of the tank, and the outermost point was considered to be the boundary separating his area from his neighbour’s. In all five replicates, the removal of the intruders caused a change in position of this “boundary” (Fig.1). Uniformly, one male began to expand his territory at the expense of his neighbours. However, with the readdition of the conspecific intruders, the neighbour was able to reclaim at least some of his lost area. DISCUSSION
Dominance and territoriality appear inter-related, as both are derived from agonistic behaviour, and it is relatively easy to shift from one system to the other. Most laboratory analyses suggest that dominance is a result of high densities (e.g., Bennett, 1942; Greenberg, 1947; Davis, 1958), concluding that area defense occurs in times of low competition. The observed shift is, therefore, difficult to explain, since it should be inefficient to defend an unlimited
E ”
Fig.1. Territory size as related to the presence or absence of conspecific intruders. Each line represents a different male in separate territorial situations. The vertical axis represents a l-cm scale illustrating the number of centimeters gained and lost with presence (l), absence (2) and re-addition (3) of conspecific intruders.
389
resource (i.e., abundant space). Conversely, Becker and Flaherty (1968) observed that dominance relationships in rats become unstable as numbers increase. The data presented here suggest that other variables, besides density, are important determinants in predicting the social system and, cumulatively, they point to a logical fitness strategy. In pupfish, low or high densities alone cannot predict the resulting social system; the absolute area available is of equal importance. Thus, five fish may form a dominance system in small areas but the same density may be territorial with a larger area. The four factors considered here (i.e., area, numbers of males, presence of females and presence of a partial barrier), all have the common denominator of reducing the influence of the dominant on subordinates. This may occur if too many subordinates are present, preventing the dominant from effectively communicating his dominance status. Increasing the area, or adding a partial barrier, probably retarded the dominant from swimming swiftly to all parts of his area, and similarly reduced the dominant’s contact with subordinates. The presence of a receptive female appeared to heighten the competition for females disproportionately to the dominant’s ability to increase his harassment of the subordinates. I see the pupfish mating system as a balance, in which the dominant attempts to maintain its high fitness, while the subordinants attempt to increase theirs. I observed (Itzkowitz, 1974) that in a dominance system composed of two or three pupfish males, the dominant prevents the access of the subdominants to receptive females. As females deposit eggs randomly, a dominant’s fitness is directly proportional to the quantity of area he controls (Itzkowitz, in preparation). Thus, the dominant must compromise its attempts to increase its area of control since this would also increase the likelihood that it will be less effective in controlling its competitors within this larger area (see Schoener, 1971). The data presented here suggest that when intruders become numerous, the dominant’s tactic is to reduce its area (i.e., become territorial) which allows it to exclude competitors more effectively. As the dominant abandons some of the available area, subdominants will attempt to increase their fitness by forming adjacent territories. One of the predictions based on these fitness relationships is the abolishing of aggression and mating in the presence of very large numbers of competitors. Under these conditions, an individ: 71 is forced to reduce his area of dominance below the point at which the area is capable of supporting a successful mating. In large aquarium populations, I have observed this loss of mating activity in the pupfish and in a cichlid fish, Aegiudens p&her, and it has also been reported in several species of rodent (Eisenberg, 1967). I would expect, however, that species which maintain the territory, or dominance systems, for purposes other than as a mating strategy, vould introduce considerable variation in the predictive ability of this system.
390
Territoriality
in a heterogeneous
habitat
The above discussion focused on the fitness relationships of dominance and territorial behaviour in a homogeneous habitat. That is, given equally defended areas, all territorial individuals have equal fitness. With the pupfish, this relationship seems probable for uniform areas, and differences in fitness appear to be related to the size of the area defended (Itzkowitz, in preparation). It seems apparent that, in the many species studied (including the pupfish), homogeneity is unusual and those individuals residing in specific portions of a habitat may have a higher fitness than those living in other areas. I can further visualize a dominant, having his fitness challenged by subdominants, selecting the best area for territorial defense. In a heterogeneous habitat, the evolutionary and behavioural differences between the two systems are relatively minor. A dominant retreating to the most favourable portion of the habitat will continue to have a relatively higher fitness than his territorial neighbours. On a behavioural level, I expect competition for superior areas is similar to the subdominants’ challenge of the dominant. The intense competition for the more superior areas may result in these areas being smaller than inferior ones (e.g., lek centers have smaller territories than peripherals: Wiley, 1973). CONCLUSION
The territory is a natural extension of the dominance tactic to maintain a higher fitness strategy. In a homogeneous environment, the subdominants can reduce the dominant’s fitness by forcing it to become territorial. In a heterogeneous habitat, the dominant will probably select the best area and thus maintain its higher fitness. Territorials in inferior habitats will challenge the superior territorial, which could result in its retreating to a smaller area. In both environments, very high densities should result in the cessation of mating. ACKNOWLEDGEMENT
I am grateful to Robert Jaeger and R. Haven Wiley for critically reading earlier drafts of this paper.
REFERENCES Becker, G. and Flaherty, T.B., 1968. Group size as a determinant of dominance-hierarchy stability in the rat. J. Comp. Physiol. Psychol., 68: 433-476. Bennet, MA., 1942. Effects of testosterone propionate on territoriality in flocks of ringdoves. Trans. Ill. State Acad. Sci., 35: 193-194. Boice, R. and Witter, D.W., 1969. Hierarchy feeding behaviour in the leopard frog (Rana pipiens). Anim. Behav., 17: 474-479.
391
Bovberg, R.V., 1956. Some factors affecting aggressive behaviour in crayfish. Physiol. Zool., 29: 127-136. Brown, J.L., 1975. The Evolution of Behaviour. W.W. Norton & Co. Inc., New York, 761 pp. Carpenter, C.R., 1958. Territoriality: a review of concepts and problems. In: A. Roe and G.G. Simpson (Editors), Behaviour and Evolution. Yale Univ. Press, New Haven, Corm., pp. 224-250. Davis, D.E., 1958. The role of density in aggressive behaviour of house mice. Anim. Behav., 6: 207-210. Eisenberg, J.F., 1967. A comparative study in rodent ethology with emphasis on the evolution of social behaviour. Proc. U.S. Nat. Mus., 122: 1-51. Figler, M.H., Klein, R.M. and Peeke, H.V.S., 1976. The establishment and reversibility of dominance relationship in jewel fish, Hemichromis bimaculatus Gill (Pisces, Cichlidae): effects of prior exposure and prior residence situation. Behaviour, 58: 254-271. Frey, D.F. and Miller, R.J., 1972. The establishment of dominance relationship in the blue gourami, Trichogaster trichopterus (Pallas). Behaviour, 42: 8-62. Greenberg, B., 1947. Some relationships between territory, social hierarchy, and leadership in the green sunfish (Lepomis cyanellus). Physiol. Zool., 20: 267-299. Itzkowitz, M., 1974. The effects of other fish on the reproductive behaviour of the male variegated pupfish, Cyprinodon uariegatus (Pisces: Cyprinodontidae). Behaviour, 48: l-22. Phillips, R.R., 1974. The relationship between social behaviour and the use of space in the benthic fish Chasmodes bosquianus La&p&de (Teleostei, Blenniidae). III. The interactions between attraction/repulsion and prior social experience. Behaviour, 49 : 205-226. Schoener, T.W., 1971. Theory of foraging strategies. Annu. Rev. Ecol. Syst., 2: 269-404. Wiley,yR.H., 1973. Territoriality and non-random mating in sage grouse Centrocercus urophasianus. Anim. Behav. Monogr., 6: 85-169. Wilson, E.O., 1975. Sociobiology: The New Synthesis. Harvard Univ. Press, Cambridge, Mass., 697 pp.
333
Short Communication INTERRELATIONSHIPS OF DOMINANCE AND TERRITORIAL BEHAVIOUR IN THE PUPFISH, CYPRINODON VARIEGATUS M. ITZKOWITZ Department
of Zoology,
University
of the West Indies, Kingston
7 (Jamaica)
(Received 4 April 1977; revised 20 October 1977)
ABSTRACT Itzkowitz, M., 1977. Interrelationships of dominance and territorial behaviour in the pupfish, Cyprinodon variegatus. Behav. Processes, 2: 383-391. Under laboratory conditions, Cyprinodon variegatus establishes either a dominance or territorial mating system. In the dominance system, one male usually has complete access to receptive females, while in the territorial system, several males have equal access. Four factors were observed to enhance a subdominant’s ability to establish a territory and improve his reproductive success; increasing the number of conspecific intruders, increasing the available area, the presence of partial barrier, and the presence of a receptive female.
INTRODUCTION
Territorial and dominance systems serve a large variety of functions for a diverse assemblage of animal groups (Carpenter, 1958). The two systems have two basic factors in common: first, both utilize agonistic behaviour to develop and maintain them, second the dominant and the territorial defender each has the highest fitness within its area of movement (see reviews of Brown, 1975; Wilson, 1975). Theoretically, differences arise with territoriality allowing several individuals to co-exist within a unit area with potentially equal fitness, while the dominant has the highest fitness within the same area. However, if both social systems depend on the same behavioural mechanism, why would a dominant allow other individuals to share the area equally (thereby becoming territorial) and thus reduce its own fitness? Ideally, answers to such questions are best uncovered by the manipulation of specific environmental variables to induce a shift from one system to the other. Unfortunately, most studies which do consider the ecological and evolutionary consequences of these systems are performed on species (e.g., birds) that are difficult to manipulate experimentally. Cyprinodon uariegutus La&p&de, the pupfish, could shed some light on the relationships between these two systems as it can develop and maintain either a dominance or territorial system under certain laboratory conditions. This is not unusual for fish as I, (unpublished) and others (e.g., Greenberg, 1947),
384
have observed it in other species (see definitions below). As the pupfish territory appears to function only for mating, many of the other environmental pressures important for other species (e.g., distribution of food, predator protection, predation) were not considered. Here, I consider four factors which I hypothesized to be important in maintaining one or the other system; the number of intruders, the size of the available area, the presence of a partial barrier, and the presence of a receptive female. These variables were selected, as previous studies have indicated that they are influential in modifying territorial and/or dominance behaviour. DEFINITIONS
Within the confines of an aquarium or cage, it is possible to assume that a dominant is actually a territorial defending the entire area. Traditionally, it has been considered as dominance (e.g., Greenberg, 1947; Bovberg, 1956; Boice and Witter, 1969; Frey and Miller, 1972; Phillips, 1974; Figler et al., 1976), as the overt behaviour differs little between individuals confined in a territory, and one where the subordinates stay within the domain of the dominant. In both situations, the dominant can chase others but is rarely attacked, and has greater access to food and/or mates. Here I continue the traditional definition of a dominant as one that can chase any fish within the entire tank. Territoriality exists only if two or more males defend discrete areas within the same tank and each male is dominant only within its area. MATERIALS
AND METHODS
Cyprinodon uariegutus is a small, cyprinodont fish that reaches sexual maturity at 2-3 cm. The adults in this study were uniformly 40-45 mm. The sexes are dichromic, with the males having a blue irredescent dorsal region, black pectoral fins and a black bar at the edge of the caudal fin. The females are light, with large dark grey or black blotches on the sides of the body. The adults were collected from Port Henderson, Jamaica (on the western side of the entrance to Kingston Harbour), from a small shallow pool (diameter 5 m) located directly behind a sandy beach and surrounded by mangrove plants. While the pool appeared to receive water only from high tides and rain, complete drying was never observed. The specimens were gradually acclimated to freshwater over a 24-h period and then transferred to a large stock tank. After approximately 14 days at a 15-h light cycle, the fish were used in the experiments. All experiments were conducted in glass aquaria (120 X 20 X 30 cm) which were marked lengthwise at l-cm intervals. The depth of the water was 15 cm, which corresponded to the depth of natural territories (Itzkowitz, 1974). Six experiments were conducted using the above aquaria. In all instances, the position of either the dominant or territorial male was noted for a lo-min period, during which a continuous record was maintained of the male’s
385
changes in position. Normally the male made between 150 and 250 position changes during the 10 min. For some experiments an opaque glass partition divided the tank in half (“half tanks”), reducing the length to 60 cm. Experiment I. This experiment was designed to observe the influences of male numbers on the formation of a dominance or territorial system. Three densities (2, 5 and 10 males) were randomly placed in the ten half tanks and allowed to acclimate for 24 h. After acclimation the position of the dominant or territorial male was recorded for a lo-min period. After the observation, all experimental animals and those remaining in the stock tanks, were placed in a bucket and randomly redistributed for the next day’s observations. A total of 75 fish were available for the experiments. Experiment II. This experiment considered the influence of females on the formation of a dominance or territorial system. The same procedures were used here as in Experiment I, but with the addition of two resident females in each half tank. Experiment III. I hypothesized that obstructions which interfered with a dominant’s ability to move swiftly across the half tank or view all aspects of it, would influence the establishment of a territorial or dominance system. The partial barrier divided the half tank into two equal sections across the width. It consisted of a mound of sand tapered into a fine edge, and small pieces of black plastic were projected at irregular intervals along the edge. The experimental procedures used here were identical to those followed in Experiment II. Expc:,Lnent IV. I tested the influence of a larger area on the formation of a social system. The opaque dividers were removed allowing complete access to the entire tank (“full tanks”). The procedures used here follow those of Experiment I (i.e. no female residents) but there was an increase in the number of male densities (2, 5, 10 and 20 males). Experiment V. This experiment was similar to Experiment IV except for the presence of two adult females in each full tank. Experiment VI. In the last experiment I considered the influence of nonterritorial intruders on the stability of a boundary separating two territorial males. Five males were simultaneously placed in a half tank. To stimulate territory formation, a partial barrier (see above, Experiment III) was erected, dividing the substratum area in half. After 24 h two territories were formed, leaving the other three males as non-territorial intruders. Removal of the partial barrier did not immediately influence the territories, as they maintained their respective areas for at least several hours, and in most cases, for the rest of the day. The territorial position in relation to a l-cm scale was
386
recorded every 2 set for 10 min. The three intruders were then removed and after a delay of 45 min, the position of the same male was again recorded. The intruders were then replaced and after a delay of 45 min, the position of the male was recorded for a final time. This was replicated with five different groups in five different tanks. RESULTS
Experiment I. In the half tank, increasing the number of competing males did not significantly increase the appearance of territories (chi-square: P > 0.05, Table I).
TABLE
I
Presence of dominance number of replicates) Number
of males
2 5 10
or side-by-side
territories
in half tanks without
N
With territories
With dominance
5 6 6
0 1 2
5 5 4
females
(N =
Experiment II. The addition of receptive females to the half tanks did not significantly increase the appearance of territories (chi-square: P > 0.05, Table II). There was no significant difference between the number of territories formed in Experiments I and II (chi-square: P > 0.05).
TABLE Presence Number 2 5 10
II of dominance*or of males
territories
in half tanks with females
N
With territories
With dominance
6 6 6
0 0 1
6 6 5
(N = number
of replicates)
Experiment III. The addition of a partial barrier to the half tanks significantly increased the total number of territorial situations in this experiment as compared to Experiment II (chi-square: P < 0.05, Table III). However, within this experiment, increasing the number of males did not influence territory formation. At all densities, a maximum of two territories formed, with most utilizing the barrier as the boundary separating the two defended areas.
387
TABLE III Presence of dominance or territories imhalf tanks with a partial barrier; females were present (N = number of replicates) Number of males
N
Territories
Dominance
2 5 10
6 6 6
3 5 4
3 1 2
Experiment IV. Doubling the available area, by removing the opaque partition, produced significantly more territorial situations (excluding the 20-male density) than the non-barrier experiment (I) (chi-square: P < 0.05, Table IV). There were significantly more territories formed at the higher densities (10 and 20) than at the lower densities (2 and 5) (Fisher test: P = 0.01, two tailed).
TABLE IV Full tanks (double area); without females (N = number of replicates) Number of males
N
Territories
Dominance
2 5 10 20
5 6 6 6
0 2 6 6
5 4 0 0
Experiment V. With the addition of females, there was a significant increase (chi-square: P < 0.05) in the number of territories formed at the low densities as compared to Experiment IV (Table V).
TABLE V Full tanks with females Number of males
N
Territories
Dominance
2 5 10 20
6 6 6 6
4 5 6 6
2 1 0 0
388
Experiment, VI. The 300 position points recorded for a male revealed that the boundaries separating the two males had no sharp demarcation. Thus, the outermost limit of a male’s movement often over-lapped with the outermost movement of his neighbour. As there was no sharp boundary line, direct measures of boundary changes were not possible. An alternative procedure used was to calculate the area within which the male confined 80% of his movements. The calculation entailed the number of times the male was observed at a l-cm mark and began at the furthest point from his territorial neighbour. Thus the first l-cm mark was closest to the end of the tank, and the outermost point was considered to be the boundary separating his area from his neighbour’s. In all five replicates, the removal of the intruders caused a change in position of this “boundary” (Fig.1). Uniformly, one male began to expand his territory at the expense of his neighbours. However, with the readdition of the conspecific intruders, the neighbour was able to reclaim at least some of his lost area. DISCUSSION
Dominance and territoriality appear inter-related, as both are derived from agonistic behaviour, and it is relatively easy to shift from one system to the other. Most laboratory analyses suggest that dominance is a result of high densities (e.g., Bennett, 1942; Greenberg, 1947; Davis, 1958), concluding that area defense occurs in times of low competition. The observed shift is, therefore, difficult to explain, since it should be inefficient to defend an unlimited
E ”
Fig.1. Territory size as related to the presence or absence of conspecific intruders. Each line represents a different male in separate territorial situations. The vertical axis represents a l-cm scale illustrating the number of centimeters gained and lost with presence (l), absence (2) and re-addition (3) of conspecific intruders.
389
resource (i.e., abundant space). Conversely, Becker and Flaherty (1968) observed that dominance relationships in rats become unstable as numbers increase. The data presented here suggest that other variables, besides density, are important determinants in predicting the social system and, cumulatively, they point to a logical fitness strategy. In pupfish, low or high densities alone cannot predict the resulting social system; the absolute area available is of equal importance. Thus, five fish may form a dominance system in small areas but the same density may be territorial with a larger area. The four factors considered here (i.e., area, numbers of males, presence of females and presence of a partial barrier), all have the common denominator of reducing the influence of the dominant on subordinates. This may occur if too many subordinates are present, preventing the dominant from effectively communicating his dominance status. Increasing the area, or adding a partial barrier, probably retarded the dominant from swimming swiftly to all parts of his area, and similarly reduced the dominant’s contact with subordinates. The presence of a receptive female appeared to heighten the competition for females disproportionately to the dominant’s ability to increase his harassment of the subordinates. I see the pupfish mating system as a balance, in which the dominant attempts to maintain its high fitness, while the subordinants attempt to increase theirs. I observed (Itzkowitz, 1974) that in a dominance system composed of two or three pupfish males, the dominant prevents the access of the subdominants to receptive females. As females deposit eggs randomly, a dominant’s fitness is directly proportional to the quantity of area he controls (Itzkowitz, in preparation). Thus, the dominant must compromise its attempts to increase its area of control since this would also increase the likelihood that it will be less effective in controlling its competitors within this larger area (see Schoener, 1971). The data presented here suggest that when intruders become numerous, the dominant’s tactic is to reduce its area (i.e., become territorial) which allows it to exclude competitors more effectively. As the dominant abandons some of the available area, subdominants will attempt to increase their fitness by forming adjacent territories. One of the predictions based on these fitness relationships is the abolishing of aggression and mating in the presence of very large numbers of competitors. Under these conditions, an individ: 71 is forced to reduce his area of dominance below the point at which the area is capable of supporting a successful mating. In large aquarium populations, I have observed this loss of mating activity in the pupfish and in a cichlid fish, Aegiudens p&her, and it has also been reported in several species of rodent (Eisenberg, 1967). I would expect, however, that species which maintain the territory, or dominance systems, for purposes other than as a mating strategy, vould introduce considerable variation in the predictive ability of this system.
390
Territoriality
in a heterogeneous
habitat
The above discussion focused on the fitness relationships of dominance and territorial behaviour in a homogeneous habitat. That is, given equally defended areas, all territorial individuals have equal fitness. With the pupfish, this relationship seems probable for uniform areas, and differences in fitness appear to be related to the size of the area defended (Itzkowitz, in preparation). It seems apparent that, in the many species studied (including the pupfish), homogeneity is unusual and those individuals residing in specific portions of a habitat may have a higher fitness than those living in other areas. I can further visualize a dominant, having his fitness challenged by subdominants, selecting the best area for territorial defense. In a heterogeneous habitat, the evolutionary and behavioural differences between the two systems are relatively minor. A dominant retreating to the most favourable portion of the habitat will continue to have a relatively higher fitness than his territorial neighbours. On a behavioural level, I expect competition for superior areas is similar to the subdominants’ challenge of the dominant. The intense competition for the more superior areas may result in these areas being smaller than inferior ones (e.g., lek centers have smaller territories than peripherals: Wiley, 1973). CONCLUSION
The territory is a natural extension of the dominance tactic to maintain a higher fitness strategy. In a homogeneous environment, the subdominants can reduce the dominant’s fitness by forcing it to become territorial. In a heterogeneous habitat, the dominant will probably select the best area and thus maintain its higher fitness. Territorials in inferior habitats will challenge the superior territorial, which could result in its retreating to a smaller area. In both environments, very high densities should result in the cessation of mating. ACKNOWLEDGEMENT
I am grateful to Robert Jaeger and R. Haven Wiley for critically reading earlier drafts of this paper.
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