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Does part reproductive history predict competitive interactions and male mating success in pupfish?
A&n.
Beha.,
1995,50, 1433-1440
Does past reproductive history predict competitive interactions and male mating success in pupfish? ASTRID Department (Received final
KODRIC-BROWN
of Biology,
10 August acceptance
University
of New
Mexico
1994; initial acceptance 26 November 1994; 9 March 1995; MS. number: A7228R)
Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males’ ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating successthan PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success.Only males in good physical condition achieve high mating success,and both intra- and inter-sexual selection are important in maintaining the closecorrelation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females. Abstract.
0 1995 The Association
Many breeding systems, especially leks, are characterized by a skewed distribution of mating success:a few males mate with many females, but most males acquire few or no matings (e.g. Balmford et al. 1992). Characteristics of males that often correlate positively with dominance and high mating successare large size, good physical condition and ability to invest in energetically expensive displays (Clutton-Brock et al. 1982; Bisazzaet al. 1989; Vehrencamp et al. 1989; Green 1991; Cherry 1993). Dominance hierarchies and positions on leks are maintained through constant probing and competitive interactions with other males. Often both intra-sexual and inter-sexual selection are important selective agents in the evolution of secondary sexual traits of males. The respective roles of these two types of sexual selection in the evolution of sexually dimorphic traits are often difficult to sort out because they may act simultaneously and synergistically on the same Correspondence:A. Kodric-Brown, Department of Biology,Universityof New Mexico, Albuquerque,NM 37131,U.S.A. (email: [email protected]). 0003-3472/95/121433+08
$12.00/O
for the Study of Animal
Behaviour
trait (Conner 1989). The usual approach has been to examine a suite of male traits and determine the relative role of intra- and inter-sexual selection on their expression (Moore 1990; Warner & Schultz 1992). Usually, because of constraints imposed by the organism’s breeding system, only males actively defending territories are considered. An alternative approach is to examine characteristics of a subset of males from the two extremes of the male distribution, which can easily be separated by their past reproductive history. In this study I examined a suite of behavioural and morphological traits in pupfish, Cyprinodon pecosensis, and asked how they differed between two types of males, namely, territorial individuals with a high mating success,and males that did not defend territories and engaged in opportunistic sneak spawning, a low-fitness mating tactic. I examined their function both in male-male interactions and in female choice under controlled experimental conditions. Specifically, I addressed the following questions. (1) How does past social status affect the development of nuptial coloration and agonistic interactions with other males? (2) In the absence of male-male interactions and
0 1995 The Association 1433
for the Study
of Animal
Behaviour
Animal
1434
Behaviour,
controlling for territory quality, can females discriminate between previously territorial (PT) and previously non-territorial (PNT) males? The experiments were designed to test two hypotheses regarding patterns of female mate choice. (1) Male quality. Controlling for size, because larger males usually have an advantage over smaller ones (Clutton-Brock et al. 1982; Bisazza et al. 1989; Beaugrand et al. 1991; Turner 1994), territorial males are inherently of better phenotypic and genotypic quality. Thus they should win agonistic encounters against nonterritorial males, be better able to attract females, and have a higher spawning success than nonterritorial males. Territorial males should court more and develop a more intense nuptial coloration than non-territorial males. Controlling for territory quality, females should choose males based on their physical and/or behavioural characteristics (activity, courtship, nuptial coloration or some trait correlated with or reflecting physical condition) and they should preferentially mate with territorial rather than non-territorial males. (2) Territory quality. Often male characteristics and the resources they control are positively correlated (Thornhill 1987; Wiley 1991; Grahn et al. 1993). In pupfish, male spawning success is positively correlated with territory quality, which explains a large proportion of male mating success (Kodric-Brown 1983). Thus male spawning success may be simply an expression of the preference of females for high-quality oviposition substrates rather than a direct response to the males themselves. If female choice is based solely on territory quality, then if males are provided with territories of equal quality, previously territorial males should have the same mating success as nonterritorial males. GENERAL
Natural
History
MATERIALS METHODS
AND
of the Study Organism
The breeding system of pupfish has been characterized as a lek (Loiselle & Barlow 1978), because males compete vigorously for small territories on restricted breeding sites and only a small proportion of adult males in the population breed. The remaining males are unable to secure territories and either do not reproduce at all, or engage in sneak matings, a low-fitness reproductive tactic
50, 6
(Kodric-Brown 1986). Territorial males defend territories over substrates preferred by females as oviposition sites (Kodric-Brown 1977). Females visit male territories, deposit one to several demersal and cryptic eggs and then leave. Territorial males acquire a bright blue nuptial coloration, which intensifies during spawning activity and agonistic interactions. Males without territories do not engage in agonistic behaviour and retain the female-like colour pattern of olive-brown background with dark vertical bars, characteristic of all individuals at other times of the year. Because males compete for limited breeding habitat, male-male competition should predict subsequent male mating success. Controlling for male size, territorial males are heavier, show greater swimming endurance, and are in better physical condition than non-territorial males (Kodric-Brown & Nicoletto 1993). Methods 1 obtained fish from Mirror Lake, Bottomless Lakes State Park, New Mexico. I collected territorial males from their territories with an umbrella net. Non-territorial males and females were captured with minnow traps baited with dog food, which were placed on silty substrates where both sexes form large feeding aggregations. Territorial males, non-territorial males and females were separated and held for 1 week in large fibreglass tanks (1.8 m in diameter) at relatively high densities of 80 individuals per tank for the following reasons. (1) At least some of the non-breeding males may be spawned-out individuals that have temporarily left their territories to recover their body reserves (Otis & Itzkowitz 1984). If so, then a week of ad libitum feeding should minimize differences in weight and general body condition between territorial and non-territorial males. (2) Outcomes of prior social encounters may affect subsequent dominance, so that previous winners are more likely to win subsequent contests (Franck & Ribowski 1989; Beaugrand et al. 1991). Then placing territorial males for a week under conditions where they cannot defend territories should eliminate expression of nuptial coloration and minimize, although perhaps not entirely eliminate, effects of prior dominance. (3) Females were separated from males and kept on an ad libitum diet for a week to ensure that they would be gravid during the female choice experiments.
Kodric-Brown: Male mating successin pupfish All experiments were conducted outdoors at the National Fish Hatchery at Dexter, New Mexico, from 6 June to 24 July 1991, which coincided with the peak of the breeding season of pupfish in the lake. I used nine fibreglass tanks (1.2 m in diameter) for all experimental manipulations. The bottom of each tank was covered with 5 cm of silica sand. Two rocks, 8 cm in diameter, provided focal sites for territories. All observations were taken from a platform, suspended by scaffolding, 2.5 m above the tanks. Behaviour of fish was recorded for two consecutive 30-min periods with a data logger (IBM portable computer) and videotaped on SVHS tape with a Panasonic camcorder. Values for the two periods were averaged, and analyses were performed on these averages. After each trial, the sand in the experimental tanks was vacuumed and new rocks were placed on the substrate to remove potential odour cues from previously deposited eggs. Descriptions of agonistic behaviour, such as frontal and lateral displays and fights, follow those of Barlow (1961). Courtship behaviour consistsof a seriesof circling movements below a female, in which the male attempts to lead the female to an oviposition site on his territory (Liu 1969). Spawning is characterized by a series of S-shaped movements by the spawning pair, following by jerking, which results in the releaseof sperm by the male and a single egg by the female. Male mating successwas estimated by recording the number of females that mated with a focal male and the number of eggs fertilized per spawning sequence. Number of eggs fertilized per spawning sequence was assessed indirectly by counting the number of jerking movements performed by the spawning pair. Eggs were not collected after a trial, because they are transparent, are hidden in cracks and crevices of rocks, and are thus difficult to recover. Male activity was estimated. by instantaneously recording at 5-min intervals throughout a 30-min observation period, whether a male was actively swimming (1) or stationary (0). These values were summed over the observation period and divided by the number of intervals (6). Male nuptial coloration was quantified by constructing a five-category colour-score index: from 1 (least developed and most femalelike) to 5 (most developed and a bright iridescent blue; Kodric-Brown & Mazzolini 1992). Colour scoresfor each focal male were recorded at 5-min
1435
intervals, summed and divided by the number of intervals (6). Both males and females used in the experiments were tested only once. After a trial each male was anaesthetized with MS222, then transferred into an individually labelled vial filled with 80% isopropyl alcohol. All males were weighed on an analytical balance to the closest 0.01 g, and standard length measurements were taken with digital callipers accurate to 0.01 mm. Females were released into the lake. Paired Wilcoxon signed-ranks tests were used for the analyses, because behavioural data were not normally distributed. A paired f-test was used to analyse differences in male weights.
PRIOR BREEDING STATUS AND PHYSICAL CONDITION I tested the hypothesii that PNT males represent spawned-out individuals that are actively feeding and recouping their resources to engage in another reproductive episode. Methods Weight measurements were taken on paired males used in the male-male interaction and female choice trials. There were 54 PT-PNT male pairs (14 from the male-male interaction trials and 40 from the female choice trials). Results The average ( f SE) weight of PT males was 1.136 & 0.02 g, whereas PNT males weighed 1.139 f 0.02 g. There were no statistically significant differences in the weights of the two types of males (paired t=0.27, df=53, P=O.78).
EXPERIMENT 1: INTRA-SEXUAL INTERACTIONS AND PRIOR BREEDING STATUS Methods Agonistic encounters were staged between a PT and a PNT male, visually matched for size (within f 0.3 mm standard length). Trials were conducted in fibreglass tanks divided in half with
Animal
1436
Behaviour,
markings on the body and differences in the colour of the pectoral and pelvic fins. I conducted 14 trials. Both males and females were replaced after each trial.
Male dominance
Opaque Plexiglas
Results
\ Rock
1
120 cm
J
Female dominance
L-4 16QQ
1
50, 6
120 cm
J Figure 1. Diagram for the set-up of the male-male interaction and the female-choice experiment (see text). PT: Previously territorial male; PNT: previously nonterritorial male. opaque partitions (Fig. 1). I introduced 16 females into the compartment, allowed them to acclimate for 15 min, then simultaneously introduced the two test males into the compartment. Observations were begun after a 30-min acclimation period. Because males were matched for size, individuals were identified by unique melanin
Past social status and breeding condition determined the outcomes of staged encounters between PT and PNT males (Table I). PT males chased more often than PNT males (100% of trials). They also developed a more intense nuptial coloration (100% of trials). The outcome of agonistic interactions was established during the first 30-min observation period (Table I). By the second 30-min observation period all chases were initiated by the PT male (X* SE= 15.8 f 0.17), who also defended both rocks and kept the subordinate, PNT male near the surface of the tank. Previously non-territorial males did not initiate any chases during the second 30-min observation period. EXPERIMENT 2: INTER-SEXUAL INTERACTIONS AND PRIOR BREEDING STATUS Methods Each fibreglass tank was divided in half with a O.&cm2 mesh hardware cloth. One half of the tank was further subdivided into two compartments with an opaque partition. The two compartments were identical in size and in topography (Fig. 1). I introduced a PT and a PNT male, matched for size ( + 0.3 mm standard length), one into each compartment. The opaque partition between the two compartments prevented visual interactions between males. I placed 16 females into the large compartment behind the wire mesh screen and a removable opaque partition which temporarily separated them from the two males. I began observations after a 30-min acclimation period.
Table I. Mean ( * SE) values of agonistic interactions and nuptial coloration of 14 pairs of previously territorial (PT) and previously non-territorial (PNT) males of C. pecosensis
variable Size (mm) Chase Colour score
PT males 33.1 zt0.36
17.3 f 1.66 2.3 f 0.16
PNT males
3
33.0 f 0.42 0.9 f 0.31 1.5zto.19
0.31 4.52 3.60
P 0.83
0.0001 0.009
Kodric-Brown:
Male mating success in pupjish
1431
Table II. Mean ( * SE) values of activity, courtship behaviour, nuptial coloration and spawning successof 40 pairs of previously territorial (PT) and previously non-territorial (PNT) males of C. pecosensis Variable
PT males
PNT males
z
P
Size (mm) Activity Courtship Colour score No. of females attracted No. of females attracted during first 5-min of observation No. of spawns Attempted spawns Eggs/spawn Time to spawn (min)
36.14 f 0.19 1.07ZLo.13
36.16+0.18 0.71 f 0.05
0.11 4.91
0.92 co.ooo1
9.08 LIZ0.93
3.55 f 0.94
1.43*0.11
3.64 f 0.35
2.29 c!c 0.23
4.83 3.92 3.05
<0.0001
2.01 Z!L0.14 3.36*
2.54 f 0.34
2.50 5.95 3.05 5.79 2.24
0.01 ~0.0001 0.01 ~0.0001
0.25
10.37 + 1.76 1.33 * 0.33 4.86 f 0.43
10.60 f 1.27
The opaque partition separating the females from the males were removed. Females could enter and leave the males’ compartments at will through openings in the screen, but the larger males were restricted to their respective compartments (Fig. 1). I recorded the number of females in a male’s compartment, spawning bouts, eggs laid per spawning bout, attempted spawnings, courtship behaviour, male activity and colour” score throughout two 30-min observation periods. I conducted 40 trials.
1.35 f 0.45 0.55 f0.23 1.74 f 0.77 13.55 f 1.27
~0.0001 0.002
0.02
T
T 7
E 8m 1.8 2 2 1.6 s 1.4
Results Females preferentially visited the compartment of the PT male (Table II; 85% of trials). Previously territorial males were more active (65% of trials), courted more vigorously (93% of trials), spawned with a greater number of females (95% of trials), and fertilized a greater number of eggs per spawning bout (93% of trials) than PNT males. There were few trials in which females preferentially visited the compartment of PNT males (N=4), or where PNT males were more active (N=l), courted more vigorously (N=3), spawned with a greater number of females (N=2), or fertilized a greater number of eggs (N=3) than PT males. Previously territorial males also developed a more intense nuptial coloration than PNT males in 80% of the trials. Previously non-territorial males were showier than PT males in four trials. Although at the beginning of each trial both types of males were female-like, with a colour score of 1, PT males developed a more intense nuptial coloration more quickly than PNT males (Fig. 2).
0
5
6
Period Figure 2. Changes in the intensity of breeding coloration of previously territorial (m) and previously nonterritorial males (0) of C. pecosensis, measured at 5-min intervals during the first 30-min observation period of the female choice experiment.
DISCUSSION The results of both the male-male interaction and the female choice experiments supported the predictions of the male quality but not the territory quality hypothesis. Prior breeding status and previous possession of a breeding territory predicted the outcome of staged interactions between males. Even under conditions of reduced competition between two males matched for size and each defending a separate patch of spawning substrate,
1438
Animal Behaviour, SO,6
PT males were invariably dominant over PNT males. In the mate choice trials females discriminated between the two types of males and actively chose the PT male over the PNT male. Females presumably based choice on behavioural and colour differences, because male size and territory quality were both controlled for. The weight analysis suggests that differences in competitive ability and attractiveness to females could not be attributed to differences in the body mass of PT and PNT males. It also indicates that if PNT males initially weighed lessthan PT males, as suggested by a field study by Kodric-Brown & Nicoletto (1993), these differences disappeared during the week of ad libitum feeding. Thus the data do not support the hypothesis that at any one time a substantial number of the non-territorial males are individuals that have bred previously and are recovering. However, other physiological differences between males could have resulted in differences in activity, behaviour and mating successbetween PT and PNT males. Territorial males and non-territorial males collected directly from Mirror Lake differ in their swimming endurance, which is an indicator of overall physical condition (Kodric-Brown & Nicoletto 1993). There are several additional explanations for the observed differences between PT and PNT males. Although the current experiments were not designed to distinguish between those mechanisms, the results permit some assessmentof their possible roles. The outcomes of prior agonistic encounters affect the behaviour of protagonists in subsequent encounters (e.g. Franck & Ribowski 1989; Beaugrand et al. 1991; Keeley & Grant 1993). It is unlikely, given the size of the lake and the male population, that the two males tested in staged encounters had a previous history of interaction on the breeding ground in the field. Past social experience could still affect subsequent behaviour in a more generalized way, however. For example, physiological mechanisms, such as elevated androgen levels, may cause higher levels of activity and aggression (Fernald 1976; Zielinski & Vandenbergh 1993). Because PT males won numerous encounters with intruders and territorial neighbours with contiguous territories and spawned with females, their prior dominance and mating success could have affected their subsequent behaviour in staged male-male and female choice trials. Thus the possibility exists that
differences between the two types of males in dominance and the ability to attract females may have been conditioned by previous history of dominance or subordinance. The female copying hypothesis proposes that the observed skew in male mating successmay be due to females copying the previous mate choice of other, often older and more experienced females (Losey et al. 1986; Dugatkin 1992; Gibson & Hoglund 1992). In the female choice experiment, females had the opportunity to observe the activities of other females and to follow them into male compartments. Significantly more females visited the compartment of the PT male during the first 5 min of the trial (Table II). If differences in male mating successwere largely due to female copying, then the first male to mate with females would have a higher mating success,irrespective of his past territorial status. This was not the case, because PT males spawned sooner than PNT males (10.6 min versus 13.6 min, respectively; Table II). Also, the number of females in a male’s compartment during the 5-min period before a spawning and the 5-min period after a spawning did not differ, as it should have if females were observing mating activities of males and copying the mate choice of other females (zberore=3.6. X,&-ter=4.1,-7=1.84, N=65 pairs, P
Kodric-Brown:
Male mating success in pupfish
and as a signal to females, because it is expressed in the absence of male-male interactions (experiment 2). Both PT and PNT males developed nuptial coloration under appropriate social circumstances and it intensified after spawning bouts; thus, nuptial coloration is a conditiondependent and phenotypically plastic trait. It is an honest indicator of male quality that reflects past reproductive and agonistic behaviour. Models of epigamic sexual selection either focus on the ornament itself as the target of female choice, or emphasize the close interaction between an ornament and traits that reflect a male’s constitution and general health. Fisherian models posit that female preference evolves as a correlated response to selection on the ornament (Fisher 1958; Lande 1981; Kirkpatrick 1982; Heisler 1985). Such ornaments function as aesthetic displays, and provide no information about male quality. Good genes models propose that variation in the expression of the secondary sexual trait is conditional, and reflects a male’s phenotypic and presumably genotypic quality. Thus although the proximate< focus of female choice is on the degree of elaboration of a male’s secondary sexual trait, sexual selection acts to produce alrPi maintain the trait based on the accuracy with which it expresses male quality (Kodric-Brown & Brown 1984; Andersson 1986; Pomiankowski 1988; Hasson 1989; Iwasa et al. 1991). Examples of secondary sexual traits that are affected by male condition are the expression of carotenoid pigment in fish and birds (e.g. Kodric-Brown 1989; Hill 1991; Houde & Torio 1992), the size and symmetry of an ornament (Mplller 1990; Watson & Thornhill 1994) or the vigour of a display (Vehrencamp et al. 1989). The utility of such conditionally expressed secondary sexual traits to females depends on how accurately they reflect male quality. Because both social and environmental conditions change during a single breeding season or between breeding seasons, conditionally expressed traits that vary in intensity and can be rapidly turned on or off are likely to be used by females as indicators of male quality. Thus sexual selection should favour the evolution of courtship and secondary sexual traits, such as the nuptial coloration in pupfish, which accurately signal not only past mating success but also past aggressive dominance. Such traits should act as amplifiers (sensu bsson 1989) in that they accentuate differences in nmwm
1439
Initially, even in the absence of nuptial coloration, females were able to differentiate between PT and PNT males based on other male attributes, such as activity and courtship. During the course of the trial these initial differences between the PT and PNT male became more pronounced as the PT males developed a more intense nuptial coloration, which reflected a history of spawning activity (Fig. 2). The results of these experiments indicate that female choice is not arbitrary, even under the conditions of these experiments, which deliberately equalized between the competing males many physical, social and environmental f~tors known to affect male mating success.
ACKNOWLEDGMENTS I am grateful to the statf at the Dexter Fish Hatchery for generously providing tClitics for setting up the experiments, to my assistant D. Boyd for assistance in the lield, to P. N/~~ilc‘::,: for data analysis, to J. Brown, the behaviourai ecology discussion group at U.N.M.. to P. Schwagmeyer and an anonymous rcrcrec Ihr trillcal comments and valuable suggestion3 on the manuscript. This research was supporled by NSI. grant BNS-8808109.
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Beha.,
1995,50, 1433-1440
Does past reproductive history predict competitive interactions and male mating success in pupfish? ASTRID Department (Received final
KODRIC-BROWN
of Biology,
10 August acceptance
University
of New
Mexico
1994; initial acceptance 26 November 1994; 9 March 1995; MS. number: A7228R)
Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males’ ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating successthan PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success.Only males in good physical condition achieve high mating success,and both intra- and inter-sexual selection are important in maintaining the closecorrelation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females. Abstract.
0 1995 The Association
Many breeding systems, especially leks, are characterized by a skewed distribution of mating success:a few males mate with many females, but most males acquire few or no matings (e.g. Balmford et al. 1992). Characteristics of males that often correlate positively with dominance and high mating successare large size, good physical condition and ability to invest in energetically expensive displays (Clutton-Brock et al. 1982; Bisazzaet al. 1989; Vehrencamp et al. 1989; Green 1991; Cherry 1993). Dominance hierarchies and positions on leks are maintained through constant probing and competitive interactions with other males. Often both intra-sexual and inter-sexual selection are important selective agents in the evolution of secondary sexual traits of males. The respective roles of these two types of sexual selection in the evolution of sexually dimorphic traits are often difficult to sort out because they may act simultaneously and synergistically on the same Correspondence:A. Kodric-Brown, Department of Biology,Universityof New Mexico, Albuquerque,NM 37131,U.S.A. (email: [email protected]). 0003-3472/95/121433+08
$12.00/O
for the Study of Animal
Behaviour
trait (Conner 1989). The usual approach has been to examine a suite of male traits and determine the relative role of intra- and inter-sexual selection on their expression (Moore 1990; Warner & Schultz 1992). Usually, because of constraints imposed by the organism’s breeding system, only males actively defending territories are considered. An alternative approach is to examine characteristics of a subset of males from the two extremes of the male distribution, which can easily be separated by their past reproductive history. In this study I examined a suite of behavioural and morphological traits in pupfish, Cyprinodon pecosensis, and asked how they differed between two types of males, namely, territorial individuals with a high mating success,and males that did not defend territories and engaged in opportunistic sneak spawning, a low-fitness mating tactic. I examined their function both in male-male interactions and in female choice under controlled experimental conditions. Specifically, I addressed the following questions. (1) How does past social status affect the development of nuptial coloration and agonistic interactions with other males? (2) In the absence of male-male interactions and
0 1995 The Association 1433
for the Study
of Animal
Behaviour
Animal
1434
Behaviour,
controlling for territory quality, can females discriminate between previously territorial (PT) and previously non-territorial (PNT) males? The experiments were designed to test two hypotheses regarding patterns of female mate choice. (1) Male quality. Controlling for size, because larger males usually have an advantage over smaller ones (Clutton-Brock et al. 1982; Bisazza et al. 1989; Beaugrand et al. 1991; Turner 1994), territorial males are inherently of better phenotypic and genotypic quality. Thus they should win agonistic encounters against nonterritorial males, be better able to attract females, and have a higher spawning success than nonterritorial males. Territorial males should court more and develop a more intense nuptial coloration than non-territorial males. Controlling for territory quality, females should choose males based on their physical and/or behavioural characteristics (activity, courtship, nuptial coloration or some trait correlated with or reflecting physical condition) and they should preferentially mate with territorial rather than non-territorial males. (2) Territory quality. Often male characteristics and the resources they control are positively correlated (Thornhill 1987; Wiley 1991; Grahn et al. 1993). In pupfish, male spawning success is positively correlated with territory quality, which explains a large proportion of male mating success (Kodric-Brown 1983). Thus male spawning success may be simply an expression of the preference of females for high-quality oviposition substrates rather than a direct response to the males themselves. If female choice is based solely on territory quality, then if males are provided with territories of equal quality, previously territorial males should have the same mating success as nonterritorial males. GENERAL
Natural
History
MATERIALS METHODS
AND
of the Study Organism
The breeding system of pupfish has been characterized as a lek (Loiselle & Barlow 1978), because males compete vigorously for small territories on restricted breeding sites and only a small proportion of adult males in the population breed. The remaining males are unable to secure territories and either do not reproduce at all, or engage in sneak matings, a low-fitness reproductive tactic
50, 6
(Kodric-Brown 1986). Territorial males defend territories over substrates preferred by females as oviposition sites (Kodric-Brown 1977). Females visit male territories, deposit one to several demersal and cryptic eggs and then leave. Territorial males acquire a bright blue nuptial coloration, which intensifies during spawning activity and agonistic interactions. Males without territories do not engage in agonistic behaviour and retain the female-like colour pattern of olive-brown background with dark vertical bars, characteristic of all individuals at other times of the year. Because males compete for limited breeding habitat, male-male competition should predict subsequent male mating success. Controlling for male size, territorial males are heavier, show greater swimming endurance, and are in better physical condition than non-territorial males (Kodric-Brown & Nicoletto 1993). Methods 1 obtained fish from Mirror Lake, Bottomless Lakes State Park, New Mexico. I collected territorial males from their territories with an umbrella net. Non-territorial males and females were captured with minnow traps baited with dog food, which were placed on silty substrates where both sexes form large feeding aggregations. Territorial males, non-territorial males and females were separated and held for 1 week in large fibreglass tanks (1.8 m in diameter) at relatively high densities of 80 individuals per tank for the following reasons. (1) At least some of the non-breeding males may be spawned-out individuals that have temporarily left their territories to recover their body reserves (Otis & Itzkowitz 1984). If so, then a week of ad libitum feeding should minimize differences in weight and general body condition between territorial and non-territorial males. (2) Outcomes of prior social encounters may affect subsequent dominance, so that previous winners are more likely to win subsequent contests (Franck & Ribowski 1989; Beaugrand et al. 1991). Then placing territorial males for a week under conditions where they cannot defend territories should eliminate expression of nuptial coloration and minimize, although perhaps not entirely eliminate, effects of prior dominance. (3) Females were separated from males and kept on an ad libitum diet for a week to ensure that they would be gravid during the female choice experiments.
Kodric-Brown: Male mating successin pupfish All experiments were conducted outdoors at the National Fish Hatchery at Dexter, New Mexico, from 6 June to 24 July 1991, which coincided with the peak of the breeding season of pupfish in the lake. I used nine fibreglass tanks (1.2 m in diameter) for all experimental manipulations. The bottom of each tank was covered with 5 cm of silica sand. Two rocks, 8 cm in diameter, provided focal sites for territories. All observations were taken from a platform, suspended by scaffolding, 2.5 m above the tanks. Behaviour of fish was recorded for two consecutive 30-min periods with a data logger (IBM portable computer) and videotaped on SVHS tape with a Panasonic camcorder. Values for the two periods were averaged, and analyses were performed on these averages. After each trial, the sand in the experimental tanks was vacuumed and new rocks were placed on the substrate to remove potential odour cues from previously deposited eggs. Descriptions of agonistic behaviour, such as frontal and lateral displays and fights, follow those of Barlow (1961). Courtship behaviour consistsof a seriesof circling movements below a female, in which the male attempts to lead the female to an oviposition site on his territory (Liu 1969). Spawning is characterized by a series of S-shaped movements by the spawning pair, following by jerking, which results in the releaseof sperm by the male and a single egg by the female. Male mating successwas estimated by recording the number of females that mated with a focal male and the number of eggs fertilized per spawning sequence. Number of eggs fertilized per spawning sequence was assessed indirectly by counting the number of jerking movements performed by the spawning pair. Eggs were not collected after a trial, because they are transparent, are hidden in cracks and crevices of rocks, and are thus difficult to recover. Male activity was estimated. by instantaneously recording at 5-min intervals throughout a 30-min observation period, whether a male was actively swimming (1) or stationary (0). These values were summed over the observation period and divided by the number of intervals (6). Male nuptial coloration was quantified by constructing a five-category colour-score index: from 1 (least developed and most femalelike) to 5 (most developed and a bright iridescent blue; Kodric-Brown & Mazzolini 1992). Colour scoresfor each focal male were recorded at 5-min
1435
intervals, summed and divided by the number of intervals (6). Both males and females used in the experiments were tested only once. After a trial each male was anaesthetized with MS222, then transferred into an individually labelled vial filled with 80% isopropyl alcohol. All males were weighed on an analytical balance to the closest 0.01 g, and standard length measurements were taken with digital callipers accurate to 0.01 mm. Females were released into the lake. Paired Wilcoxon signed-ranks tests were used for the analyses, because behavioural data were not normally distributed. A paired f-test was used to analyse differences in male weights.
PRIOR BREEDING STATUS AND PHYSICAL CONDITION I tested the hypothesii that PNT males represent spawned-out individuals that are actively feeding and recouping their resources to engage in another reproductive episode. Methods Weight measurements were taken on paired males used in the male-male interaction and female choice trials. There were 54 PT-PNT male pairs (14 from the male-male interaction trials and 40 from the female choice trials). Results The average ( f SE) weight of PT males was 1.136 & 0.02 g, whereas PNT males weighed 1.139 f 0.02 g. There were no statistically significant differences in the weights of the two types of males (paired t=0.27, df=53, P=O.78).
EXPERIMENT 1: INTRA-SEXUAL INTERACTIONS AND PRIOR BREEDING STATUS Methods Agonistic encounters were staged between a PT and a PNT male, visually matched for size (within f 0.3 mm standard length). Trials were conducted in fibreglass tanks divided in half with
Animal
1436
Behaviour,
markings on the body and differences in the colour of the pectoral and pelvic fins. I conducted 14 trials. Both males and females were replaced after each trial.
Male dominance
Opaque Plexiglas
Results
\ Rock
1
120 cm
J
Female dominance
L-4 16QQ
1
50, 6
120 cm
J Figure 1. Diagram for the set-up of the male-male interaction and the female-choice experiment (see text). PT: Previously territorial male; PNT: previously nonterritorial male. opaque partitions (Fig. 1). I introduced 16 females into the compartment, allowed them to acclimate for 15 min, then simultaneously introduced the two test males into the compartment. Observations were begun after a 30-min acclimation period. Because males were matched for size, individuals were identified by unique melanin
Past social status and breeding condition determined the outcomes of staged encounters between PT and PNT males (Table I). PT males chased more often than PNT males (100% of trials). They also developed a more intense nuptial coloration (100% of trials). The outcome of agonistic interactions was established during the first 30-min observation period (Table I). By the second 30-min observation period all chases were initiated by the PT male (X* SE= 15.8 f 0.17), who also defended both rocks and kept the subordinate, PNT male near the surface of the tank. Previously non-territorial males did not initiate any chases during the second 30-min observation period. EXPERIMENT 2: INTER-SEXUAL INTERACTIONS AND PRIOR BREEDING STATUS Methods Each fibreglass tank was divided in half with a O.&cm2 mesh hardware cloth. One half of the tank was further subdivided into two compartments with an opaque partition. The two compartments were identical in size and in topography (Fig. 1). I introduced a PT and a PNT male, matched for size ( + 0.3 mm standard length), one into each compartment. The opaque partition between the two compartments prevented visual interactions between males. I placed 16 females into the large compartment behind the wire mesh screen and a removable opaque partition which temporarily separated them from the two males. I began observations after a 30-min acclimation period.
Table I. Mean ( * SE) values of agonistic interactions and nuptial coloration of 14 pairs of previously territorial (PT) and previously non-territorial (PNT) males of C. pecosensis
variable Size (mm) Chase Colour score
PT males 33.1 zt0.36
17.3 f 1.66 2.3 f 0.16
PNT males
3
33.0 f 0.42 0.9 f 0.31 1.5zto.19
0.31 4.52 3.60
P 0.83
0.0001 0.009
Kodric-Brown:
Male mating success in pupjish
1431
Table II. Mean ( * SE) values of activity, courtship behaviour, nuptial coloration and spawning successof 40 pairs of previously territorial (PT) and previously non-territorial (PNT) males of C. pecosensis Variable
PT males
PNT males
z
P
Size (mm) Activity Courtship Colour score No. of females attracted No. of females attracted during first 5-min of observation No. of spawns Attempted spawns Eggs/spawn Time to spawn (min)
36.14 f 0.19 1.07ZLo.13
36.16+0.18 0.71 f 0.05
0.11 4.91
0.92 co.ooo1
9.08 LIZ0.93
3.55 f 0.94
1.43*0.11
3.64 f 0.35
2.29 c!c 0.23
4.83 3.92 3.05
<0.0001
2.01 Z!L0.14 3.36*
2.54 f 0.34
2.50 5.95 3.05 5.79 2.24
0.01 ~0.0001 0.01 ~0.0001
0.25
10.37 + 1.76 1.33 * 0.33 4.86 f 0.43
10.60 f 1.27
The opaque partition separating the females from the males were removed. Females could enter and leave the males’ compartments at will through openings in the screen, but the larger males were restricted to their respective compartments (Fig. 1). I recorded the number of females in a male’s compartment, spawning bouts, eggs laid per spawning bout, attempted spawnings, courtship behaviour, male activity and colour” score throughout two 30-min observation periods. I conducted 40 trials.
1.35 f 0.45 0.55 f0.23 1.74 f 0.77 13.55 f 1.27
~0.0001 0.002
0.02
T
T 7
E 8m 1.8 2 2 1.6 s 1.4
Results Females preferentially visited the compartment of the PT male (Table II; 85% of trials). Previously territorial males were more active (65% of trials), courted more vigorously (93% of trials), spawned with a greater number of females (95% of trials), and fertilized a greater number of eggs per spawning bout (93% of trials) than PNT males. There were few trials in which females preferentially visited the compartment of PNT males (N=4), or where PNT males were more active (N=l), courted more vigorously (N=3), spawned with a greater number of females (N=2), or fertilized a greater number of eggs (N=3) than PT males. Previously territorial males also developed a more intense nuptial coloration than PNT males in 80% of the trials. Previously non-territorial males were showier than PT males in four trials. Although at the beginning of each trial both types of males were female-like, with a colour score of 1, PT males developed a more intense nuptial coloration more quickly than PNT males (Fig. 2).
0
5
6
Period Figure 2. Changes in the intensity of breeding coloration of previously territorial (m) and previously nonterritorial males (0) of C. pecosensis, measured at 5-min intervals during the first 30-min observation period of the female choice experiment.
DISCUSSION The results of both the male-male interaction and the female choice experiments supported the predictions of the male quality but not the territory quality hypothesis. Prior breeding status and previous possession of a breeding territory predicted the outcome of staged interactions between males. Even under conditions of reduced competition between two males matched for size and each defending a separate patch of spawning substrate,
1438
Animal Behaviour, SO,6
PT males were invariably dominant over PNT males. In the mate choice trials females discriminated between the two types of males and actively chose the PT male over the PNT male. Females presumably based choice on behavioural and colour differences, because male size and territory quality were both controlled for. The weight analysis suggests that differences in competitive ability and attractiveness to females could not be attributed to differences in the body mass of PT and PNT males. It also indicates that if PNT males initially weighed lessthan PT males, as suggested by a field study by Kodric-Brown & Nicoletto (1993), these differences disappeared during the week of ad libitum feeding. Thus the data do not support the hypothesis that at any one time a substantial number of the non-territorial males are individuals that have bred previously and are recovering. However, other physiological differences between males could have resulted in differences in activity, behaviour and mating successbetween PT and PNT males. Territorial males and non-territorial males collected directly from Mirror Lake differ in their swimming endurance, which is an indicator of overall physical condition (Kodric-Brown & Nicoletto 1993). There are several additional explanations for the observed differences between PT and PNT males. Although the current experiments were not designed to distinguish between those mechanisms, the results permit some assessmentof their possible roles. The outcomes of prior agonistic encounters affect the behaviour of protagonists in subsequent encounters (e.g. Franck & Ribowski 1989; Beaugrand et al. 1991; Keeley & Grant 1993). It is unlikely, given the size of the lake and the male population, that the two males tested in staged encounters had a previous history of interaction on the breeding ground in the field. Past social experience could still affect subsequent behaviour in a more generalized way, however. For example, physiological mechanisms, such as elevated androgen levels, may cause higher levels of activity and aggression (Fernald 1976; Zielinski & Vandenbergh 1993). Because PT males won numerous encounters with intruders and territorial neighbours with contiguous territories and spawned with females, their prior dominance and mating success could have affected their subsequent behaviour in staged male-male and female choice trials. Thus the possibility exists that
differences between the two types of males in dominance and the ability to attract females may have been conditioned by previous history of dominance or subordinance. The female copying hypothesis proposes that the observed skew in male mating successmay be due to females copying the previous mate choice of other, often older and more experienced females (Losey et al. 1986; Dugatkin 1992; Gibson & Hoglund 1992). In the female choice experiment, females had the opportunity to observe the activities of other females and to follow them into male compartments. Significantly more females visited the compartment of the PT male during the first 5 min of the trial (Table II). If differences in male mating successwere largely due to female copying, then the first male to mate with females would have a higher mating success,irrespective of his past territorial status. This was not the case, because PT males spawned sooner than PNT males (10.6 min versus 13.6 min, respectively; Table II). Also, the number of females in a male’s compartment during the 5-min period before a spawning and the 5-min period after a spawning did not differ, as it should have if females were observing mating activities of males and copying the mate choice of other females (zberore=3.6. X,&-ter=4.1,-7=1.84, N=65 pairs, P
Kodric-Brown:
Male mating success in pupfish
and as a signal to females, because it is expressed in the absence of male-male interactions (experiment 2). Both PT and PNT males developed nuptial coloration under appropriate social circumstances and it intensified after spawning bouts; thus, nuptial coloration is a conditiondependent and phenotypically plastic trait. It is an honest indicator of male quality that reflects past reproductive and agonistic behaviour. Models of epigamic sexual selection either focus on the ornament itself as the target of female choice, or emphasize the close interaction between an ornament and traits that reflect a male’s constitution and general health. Fisherian models posit that female preference evolves as a correlated response to selection on the ornament (Fisher 1958; Lande 1981; Kirkpatrick 1982; Heisler 1985). Such ornaments function as aesthetic displays, and provide no information about male quality. Good genes models propose that variation in the expression of the secondary sexual trait is conditional, and reflects a male’s phenotypic and presumably genotypic quality. Thus although the proximate< focus of female choice is on the degree of elaboration of a male’s secondary sexual trait, sexual selection acts to produce alrPi maintain the trait based on the accuracy with which it expresses male quality (Kodric-Brown & Brown 1984; Andersson 1986; Pomiankowski 1988; Hasson 1989; Iwasa et al. 1991). Examples of secondary sexual traits that are affected by male condition are the expression of carotenoid pigment in fish and birds (e.g. Kodric-Brown 1989; Hill 1991; Houde & Torio 1992), the size and symmetry of an ornament (Mplller 1990; Watson & Thornhill 1994) or the vigour of a display (Vehrencamp et al. 1989). The utility of such conditionally expressed secondary sexual traits to females depends on how accurately they reflect male quality. Because both social and environmental conditions change during a single breeding season or between breeding seasons, conditionally expressed traits that vary in intensity and can be rapidly turned on or off are likely to be used by females as indicators of male quality. Thus sexual selection should favour the evolution of courtship and secondary sexual traits, such as the nuptial coloration in pupfish, which accurately signal not only past mating success but also past aggressive dominance. Such traits should act as amplifiers (sensu bsson 1989) in that they accentuate differences in nmwm
1439
Initially, even in the absence of nuptial coloration, females were able to differentiate between PT and PNT males based on other male attributes, such as activity and courtship. During the course of the trial these initial differences between the PT and PNT male became more pronounced as the PT males developed a more intense nuptial coloration, which reflected a history of spawning activity (Fig. 2). The results of these experiments indicate that female choice is not arbitrary, even under the conditions of these experiments, which deliberately equalized between the competing males many physical, social and environmental f~tors known to affect male mating success.
ACKNOWLEDGMENTS I am grateful to the statf at the Dexter Fish Hatchery for generously providing tClitics for setting up the experiments, to my assistant D. Boyd for assistance in the lield, to P. N/~~ilc‘::,: for data analysis, to J. Brown, the behaviourai ecology discussion group at U.N.M.. to P. Schwagmeyer and an anonymous rcrcrec Ihr trillcal comments and valuable suggestion3 on the manuscript. This research was supporled by NSI. grant BNS-8808109.
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