Determinants of male reproductive success in pupfish (Cyprinodon pecosensis)

Anim. Behav.,1983, 31, 128-137

DETERMINANTS OF MALE REPRODUCTIVE SUCCESS IN PUPFISH

(CYPRINODON PECOSENSIS) BY ASTRID K O D R I C - B R O W N

Department of Ecology and Evolutionary Biology, Universityof Arizona, Tucson, Arizona 85721 Abstract. Studies of the territorial breeding system of Cyprinodonpecosensis at Bottomless Lakes State Park, New Mexico revealed that male reproductive mating success was affected by (a) the topographic features of a territory, and (b) the intensity of male breeding coloration. The importance of male nuptial coloration was demonstrated by increased male reproductive success with intensity of colour of the same individual males ('light', 1.6 females mated per h; 'dark', 5.4 females mated per tl). A stepwise multiple regression analysis of male reproductive success as a function of breeding substrate, nuptial colour, size and agonistic behaviour indicated that topographic complexity accounted for as much as 65.4 % of the variance in male reproductive success and coloration accounted for at least an additional 12.7 % of the variance. Male size and agonistic behaviour together explained only an additional 1.8 700of the variance in reproductiye success, and thus were fairly unimportant as indicators of female choice. A high correlation between nuptial colour and reproductive success indicates that females choose males independent of the quality of their territories. For resource-based polygynous breeding systems, male access to females is determined by control of a resource essential to female reproduction, such as oviposition sites (Campanella & Wolf 1974; Emlen & Oring 1977; Borgia 1979; Lenington 1980). For such breeding systems male fitness is positively correlated with the quality of resource held and with the ability to defend it from competing males. Male-male competition should be an important selective pressure in the evolution of those male characteristics that facilitate acquisition and defence of such resources. Female choice of male characteristics also may be important in enhancing male fitness (Barlow 1968; Weatherhead and Robertson 1979; Downhower and Brown 1980; Wittenberger 1981). In several studies of polygynous breeding systems, male reproductive success, which is an operational estimator of male fitness, was correlated with certain parameters that were assumed to be accurate indicators of resource quality (Orians 1969; Thornhill 1979; Lenington 1980). However, the importance of male characteristics in addition to, or independent of resource quality cannot readily be determined in most breeding systems, especially if differences in secondary sexual characteristics among males are so small that female choice would be difficult to demonstrate. Studying a breeding system where there is variation in the quality of essential resources, in the characteristics of males, and in the size of breeding aggregates, we can determine some common denominators of female preference, and we can better understand the role of sexual

selection in the evolution of a polygynous resource-based breeding system. Here I examine reproductive success of males of Cyprinodon pecosensis as a function of the physical features of the breeding habitat, the personal characteristics of individual males, and the size of breeding aggregates.

The Breeding System

Cyprinodon are small fish that inhabit physically rigorous environments that typically contain few other fish species. Adults range in size between 20 and 50 mill standard length. Sexes are dimorphic, males are deeper bodied with steeper dorsal profiles than females. Both sexes are olive-brown with a series of dark lateral stripes, except that reproductively active males develop a brilliant blue nuptial coloration and prominent orange-yellow pectoral fins. Both sexes are promiscuous and breed with many partners. In the population I studied, virtually all reproduction takes place on male territories. Territories are established on substrates with some topographic heterogeneity (Kodric-Brown 1977). Gravid females visit these territories, spawn with the resident male after a brief courtship and deposit a small number of demersal eggs. Cyprinodon lack direct parental care of eggs and young, although the aggressive behaviour of the resident male provides indirect protection for the eggs from conspecific cannibals and heterospecific predators (Liu 1969; Loiselle, personal communication). Although pupfish are capable of breeding when only 20 mm long, most territorial males are larger (25 to 45 mm

128

KODRIC-BROWN: MALE REPRODUCTIVE SUCCESS IN PUPFISH standard length), because there is intense competition for limited breeding substrates throughout most of the relatively short breeding season (late May to early August). A more detailed description of the breeding system of C. pecosensis is presented elsewhere (KodricBrown 1977, 1978).

Study Area Observations on Cyprinodon pecosensis were made at Bottomless Lakes State Park, Chavez County, New Mexico, from 3 to 10 June and 16 to 23 July 1979. The two periods coincided approximately with the beginning and the peak of the breeding season for this population. Detailed observations of breeding males and measurements of their territories were made at two areas of the lake, designated henceforth as 'embankment' and 'introduced rocks.' The limestone embankment was 6546 cm 2 in area and ranged in depth from 15 cm in the shallows to 1 m in the offshore area, at which point it dropped off rapidly to the depths of the lake. The embankment supported the largest breeding substrate in the lake, with 14 to 18 territories. The introduced substrate consisted of eight limestone rocks, ranging in size f r o m 739 cm 2 to 1256 cm 2, placed in a homogeneous area of silty bottom at a depth of 30 cm and 1 m from shore. These rocks provided breeding substrate in an area otherwise unsuitable for breeding (Kodric-Brown 1977). Four rocks were placed singly at l m intervals, the other four rocks were arranged in a cluster. All rocks remained in place for three days, then were rearranged in such a way that those initially dispersed were grouped and vice versa. In this way each set of four rocks served as its own control. Two replicates were obtained in June and one in July. Each of the 'isolated rocks' supported from one to five territories, depending on its size and configura, tion. I have shown previously that the arrangement of territories on introduced substrates stabilizes within a day of their introduction (Kodric-Brown 1978).

Methods Breeding substrates in both areas were filmed for three consecutive days during June and July with a Beaulieu R16 movie camera with an Angenieu 10-t20 m m z o o m lens outfitted with a polarizing filter. All substrates were filmed from shore, with the camera held almost perpendicular to the water surface. A 1 5 c m metal ruler placed on the substrate at the time of filming provided

129

an accurate scale. The limestone embankment and the rocks were filmed using 200 ft rolls of K o d a k II film at eight frames per s, which allowed 15 min of uninterrupted filming. The visual field encompassed five territories on the limestone embankment and all territories on the introduced rocks. To minimize time-related and seasonal differences in the position and length of shadows, which were used in mapping microtopographic features of territories, filming times were standardized to compensate for changes in the sun's angle. Measurements of both resident males and their territories were made from cine film. Territory size was determined from patrolling movements of the resident males. The area and whenever possible, the topographic complexity of 55 territories was mapped. In June 29 territories were mapped, five on the embankment and the remainder on the rocks. Microtopographic features which consisted of crevices, ridges, small depressions and ledges, were mapped from cine film using the shadows cast by these irregularities, whose areas were then measured with a planimeter. Depth measurements were not made, since most of the surface irregularities were less than 5 m m high. Breeding coloration of territorial males also was determined from cine film and from direct observations. Males were categorized as 'dark' or 'light' according to the intensity of their breeding coloration. ' D a r k ' males were a brilliant uniform blue, which masked the dark lateral bars, and were even darker blue on the head. 'Light' males were pale blue-grey, the lateral bars appeared faded, and the head was greenish-brown. A quantitative colour score was obtained by assigning a rank of 1 to the 'light' and a rank of 2 to the 'dark' colour category, and multiplying by the number of 30 rain observation periods a male displayed that colour intensity. Thus, if a male was observed for eight periods, two as a 'light' and six as a 'dark' male, he was assigned a colour score of 14. Although males of intermediate colour were present, data were collected only on the two extremes along the colour range. Reproductive success of territorial males was indexed by mating success and was determined by recording the number of females mated by each male. Although the release of eggs was not observed, the characteristic 'jerking' of the male during a spawning act (Barlow 196I) was assumed to accompany egg release. Agonistic behaviour of territorial males was determined from the number of fights a male engaged in

ANIMAL

130

BEHAVIOUR,

during a 30 rain observation period. Territorial males were observed between 0600 and 1200 hours, when spawning was most intense. A total o f 60 h of observations were made in June and 55 h in July. The relationship between male reproductive success, microtopography, nuptial colour, size, and aggressive behaviour of males was analysed by means of a stepwise multiple regression analysis in which the independent variables were ordered according to their importance in explaining the maximum remaining variance. A log10 transformation was used on the data for reproductive success and microtopography to meet the assumptions of a normal distribution inherent in the linear model. Results Effects of Territory Quality on Male Reproductive Success A relationship between type of breeding substrate and male reproductive success has been shown for Cyprinodon (Barlow 1961; Itzkowitz 1969, 1978; Echelle 1973; Soltz 1974; KodricBrown 1977). Females of Cyprinodon pecosensis prefer to oviposit on rocky substrates, and males defending such substrates have a higher reproductive success than males with territories in other habitats. If substrate quality is the only significant component of female choice, then low variability in substrate quality should result

31,

1

in uniformity in male reproductive success. However, the variance in the reproductive success of males with territories on a particular substrate, such as the limestone embankment, was quite high (3~= 3.0; SD = • 3.4 females mated per male per h; N = 5). This suggests that female choice is based on other factors besides macrotopographic features of the habitat, unless the variance in male reproductive success is caused only by chance. Within a particular substrate it might be expected that size of a territory would be a good predictor of relative male reproductive success, since larger territories provide more oviposition substrate than smaUer ones. An analysis of the size of 38 territories established over the introduced rocks, and the reproductive success of their residents, failed to show the expected correlation (r ~ = 0.12; NS), indicating that territory size was not an important criterion in female choice. Instead, male reproductive success was positively correlated with the microtopographic heterogeneity of territories (r 2 = 0.65; P < 0.001; Fig. 1). This relationship was demonstrated for both the June and July data. Within a habitat, or type of substrate, females apparently select territories which offer the greatest number of substrate irregularities. Field observations showed that whenever females entered a territory undetected by the resident they settled on these irregularities E-z. 0 . 6 5 R.S. = 9.62 -C. 0 . 5 6 x P < 0.001

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Fig. l. Reproductive success of males of Cyprinodonpecosensisas a function of the area of topographic complexity of their territories. Based on 8 h of observations over 4 days.

KODRIC.-BROWN: MALE REPRODUCTIVE SUCCESS IN PUPFISH and oviposited there as soon as they were joined by the mate. Effects of Breeding Coloration and Aggression on M a l e Reproductive Success

Although all reproductively active males showed some development of breeding coloration, there were qualitative differences among males irrespective of breeding habitat. Males with poorly developed nuptial coloration could be seen in all breeding habitats. Individuals frequently changed from 'dark' to 'light' (or vice versa) breeding coloration during the course of a day or even during a 30-min observation period. To determine the importance of breeding coloration for individual male reproductive success, the spawnings of 30 males with territories over the introduced rocks were analysed with respect to whether males were in 'dark' or 'light' nuptial coloration. Both the proportion of time a male displayed a particular intensity of nuptial colour and his reproductive success during that time were recorded (Table I). While displaying the 'dark' breeding coloration, individuals spawned three times more often (4.7 females per male per h) than while displaying the 'light' one (1.6 females per male per h). On average, individual territorial males displayed the 'dark' breeding coloration 75% of the time that they were observed. I controlled for the effects of territory quality (microtopography) and location by examining the reproductive success of individual males as a function of the intensity of their breeding coloration. Therefore any changes in a male's reproductive success, except undetected takeover of a territory by another male, could be attributed entirely to the effects of his nuptial coloration and behaviour. Data were collected over a relatively short period of four days,

131

territories were observed almost continuously throughout periods of greatest spawning activity, and residents did not change in size. Thus it is unlikely that a takeover of the territory by another individual changed male breeding coloration. In order to determine the importance of the proportion of time spent as either a 'light' or a 'dark' male, and to determine the intensity of nuptial coloration on individual reproductive success, a quantitative colour score was obtained for each of the 30 males (see Methods). Figure 2 indicates that the longer individuals maintained a 'dark' breeding coloration, the higher their total reproductive success (r 2 = 0.64; P < 0.00t). The differences in reproductive success of males displaying different intensities of breeding coloration are not affected by the time of day or other factors, since they persist when the comparisons are between individuals with territories of different microtopographic character over the same time period (Fig. 2) as well as within individuals, when territory quality is kept constant (Table I). Agonistic behaviour of males also was positively correlated with the intensity of nuptial coloration (r e = 0.30; P < 0.05). Residents chased intruders and engaged in fights with neighbouring males more often when they were 'dark' than when they were 'light' (P < 0.05; T = 42.5; N = 21; Wilcoxon matched-pairs signed ranks test; Table I). Interacting Effects ef Topography and Breeding Coloration on Male Reproductive Success

The relative importance of microtopographic features within territories and the expression of male nuptial coloration, aggression, and size in determining male reproductive success were analysed for 29 males with territories over the introduced rocks, by means of a stepwise multiple regression analysis. This showed that

Table I. Reproductive Success and Agonistic Behaviour of Individual Territorial Males of Cyprinodon pecosensis that Varied in the Intensity of their Breeding. Coloration

*Number of fights per h while Number of males 30

Total male-hours observed 150

Mean % of time spent as 'light' male

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1.6 :k: 0.32

SD

**Number of females mated per h while

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SD

2.4 • 0.30

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SD

1.6 :]: 1.6

*P < 0.05; Wilcoxon matched pairs signed ranks test for fights; T = 42.5; N = 21. **P < 0.001; Wilcoxon matched pairs signed ranks test for spawnings; T = 1.0; N = 24. eNumbers in parentheses indicate the range.

'dark' X

SD

4.7 :]: 2.7

132

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Fig. 2. Reproductive success of territorial males of Cyprinodon pecosensis as a function of the intensity of their nuptial coloration. All males were observed for 5 h over 4 days. m i c r o t o p o g r a p h y accounted for most o f the variance in male reproductive success, perhaps as m u c h as 65.4%, whereas nuptial coloration accounted for at least an additional 12.7% o f the variance (Table II). However these figures m a y underestimate the relative importance o f nuptial coloration, because m i c r o t o p o g r a p h y and nuptial coloration were correlated with each other (Table iII). A partial correlation analysis indicated that reproductive success is correlated with m i c r o t o p o g r a p h y (r 2 = 0.473, P < 0.01) when the effect o f males' colour scores is held constant, and with nuptial colour (r 2 = 0.317, P < 0.01) when m i c r o t o p o g r a p h y is kept constant. This suggests that nuptial coloration has a large effect on reproductive success independent o f habitat quality. Aggressive behav-

iour and male size together accounted for only 1.8 700 o f the variance in male reproductive success (Table II). Effects of Size o f Breeding Aggregation on M a l e Reproductive Success

The physical dimensions o f a breeding substrate determine, in part, the n u m b e r o f territories established on it. It is possible to examine the effects of male group size on individual breeding success by manipulating the physical dimensions o f the breeding habitat. I f there is a group-advertisement effect and females preferentially visit breeding habitats that support a large n u m b e r o f territorial males, then these males should have a higher reproductive success than individuals with territories on similar

Table H. Factors Affecting Male Reproductive Success of Cyprinodon pecosensis, as Indicated by a Stepwise Multiple Regression Analysis

Variable

N

Order of inclusion

Microtopography* Colour score

29 29 29 29

1 2 3 4

Size

Fights *LOgl0 transformation.

Contribution to r z 0.6544 0.7813 0.7981 0.8007

Variance (r 2) accounted for

F

0.6544 0.1270 0.0167 0.0026

51.11 15.10 2.07 0.31

Significance P P P P

< = = =

0.001 0.001 0.162 0.581

KODRIC-BROWN: MALE REPRODUCTIVE SUCCESS IN PUPFISH

133

Table III. Pearson Correlation Coefficients between Factors Affecting Male Reproductive Success of Cyprinodonpecosensis

Variable

Microtopographyt

Reproductive successt Microtopography Colour score Fights

0.8089**

Colour score

Fights

Size

0.7971"* 0.6509*

0.4886 0.4026 0.5506*

--0.2763 --0.0687 --0.2503 0.0783

*P < 0.05, **P < 0.01. tLoglo transformation.

substrates of smaller size. To test this hypothesis, I compared the reproductive success of males with territories on rocky substrates of three size categories. The limestone embankment, that supported between 14 and 18 territorial males, was the largest breeding habitat in the lake. Rocks that were arranged in clusters of four and supported from six to eight territories, represented habitats of intermediate size. Isolated rocks that supported from one to five territories, represented the smallest available breeding habitats in the lake. To control for topographic variability as much as possible, pairwise comparisons of male reproductive success were made from the same rocks in 'clumped' and 'isolated' arrangements. Size of breeding habitat appeared to have little effect on individual male reproductive success, especially in June (Mann-Whitney U; z = 1.407; P = 0.0793; NS; Table IV), In July, males with territories on all introduced substrates spawned less frequently than those on the limestone embankment (Kolmogorov-Smirnov, Z2 = 14.46; P < 0.001). Seasonal Changes in the Breeding System

Once territories were established on a breeding substrate, there were few changes during the breeding season (Table IV). Size of a breeding substrate mostly determined the number of territorial males. A comparison of the number and arrangement of territories on the same substrates in June and July showed progressively tighter packing of territories on all available breeding substrates as the breeding season progressed, with a corresponding increase in the overlap of territorial boundaries (Table IV). The changes in the number and arrangement of territories throughout the breedmg season were especially dramatic on the introduced substrates. On some isolated rocks

the number of territorial males doubled. In addition, almost all of these substrates supported one or two temporal territories; these were defended for one or two hours in the morning, then abandoned. Residents of temporary territories were never seen spawning. Although territories did not change significantly in size over the breeding season, there was a significant decrease in the area of topographic complexity of territories in July ( t = 2 . 5 3 ; P < 0.02; Table IV). An analysis of cine film indicated a slight rearrangement as new territories were added during the breeding season. A consistent reduction in the area of topographic complexity for territories in all habitats suggests that males initially select microhabitats with maximum topographic heterogeneity. As competition for breeding habitat increases, males are forced to relinquish some of the preferred spawning sites, with a corresponding decrease in topographic heterogeneity within territories. In June all breeding habitats contained some unoccupied breeding substrate, and territories were not always contiguous. By July all breeding substrates were occupied. A reduction in the area of topographic complexity suggests that rearrangement of existing territories and the occupation of less favorable breeding microhabitat may in part account for the observed decrease in the spawning success of males with territories on introduced substrates. However, decreased reproductive success of males with territories on the introduced substrates could not be attributed solely to a decrease in topographic heterogeneity, since this parameter changed for all territories, although more so for those on isolated rocks (a 25 % reduction). It is possible that a less stable arrangement of territories, with temporary residents, made these breeding habitats less attractive to females.

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KODRIC-BROWN: MALE REPRODUCTIVE SUCCESS IN PUPFISH Discussion In species in which parental care is minimal or absent, yet mortality of the egg stage is high, female choice should reflect selection to maximize her return per reproductive investment by choosing habitats most favourable for the development and hatching of eggs. Life history theory predicts that selection should be strongest on the most vulnerable part of an organism's life cycle (Gadgil & Bossert 1970; Stearns 1977). The importance of microtopographic features as a criterion of female choice of oviposition sites indicates that predation on eggs probably is an important selective pressure affecting female fitness, especially at high population densities or in habitats with other piscine predators. Pupfish are bottom feeding omnivores and readily eat eggs of conspecifics (Soltz 1974). In the laboratory juvenile and adult C. macularius consumed unguarded eggs (Loiselle, unpublished data). Cyprinodon territories function primarily as sites for attracting females and may contain little food to sustain a male's high metabolic expenditure. A male could extend his residency by consuming a portion of the eggs laid on his territory (Rohwer 1978). Sequestering of eggs in crevices can be interpreted as an adaptation by females to reduce egg cannibalism by the resident male or by another male in the event of takeover of the territory. Unlike many resource-based polygynous breeding systems (Orians 1969; Downhower and Armitage 1971), the critical resource of pupfish (oviposition substrate) is not depleted with increased use. Consequently, there is no upper limit to the number of females a male may attract and mate with, and thus there is no decline in the quality of a male's territory throughout the breeding season owing to prior reproductive success. The observation that territories did not change significantly in size throughout the breeding season (Table IV), supports the conclusion that topographic complexity (suitable oviposition sites) rather than area itself is the critical resource characteristic that influences male reproductive success. In fishes male coloration is often an important criterion of female choice and has been shown for species with polychromatic males where differences in male coloration are genetically determined (McPhail 1969; Semler 1971; Farr 1977; Endler 1980) as well as for males in which the intensity of breeding coloration is behaviourally controlled (Noble & Curtis 1939; Carlisle 1964; Lowe-MeConnell 1956).

135

In Cyprinodon microtopography provides the most reliable estimate of territory quality but male quality, especially the intensity of breeding coloration, is also an important criterion of female choice. A high correlation between male breeding coloration and reproductive success indicates that females assess male quality independently of territory quality (Table III). Since bright males enjoy a higher reproductive success, it is not surprising that the intensity of male breeding coloration is a reliable indicator of aggression (r ~ :- 0.30; P < 0.05); otherwise the signal would be vulnerable to cheating. A male with a well developed breeding coloration is more effective at excluding eonspecifics that are also egg predators (KodricBrown 1978). Furthermore, such a male presumably is also more attractive to other females, has more eggs and is less likely to leave or be ousted from his territory. Consequently, a female ovipositing on the territory of such a male is less likely to lose a substantial portion of her eggs to cannibalism. Since eggs are cryptic and scattered throughout the territory, it is unlikely that a female could assess both a male's quality and his past reproductive success by the number of eggs already present on his territory, an option available to females of species with conspicuous eggs and/or paternal care, Since nuptial coloration becomes more pronounced immediately after spawning or winning a fight (Kodric-Brown, unpublished data), females could use this characteristic as a fairly accurate indicator of a male's reproductive success and investment in his territory. The significant differences in reproductive success that corresponded to the intensity of male breeding coloration (Tables I, II, Fig. 2) suggest that conspicuousness on a territory is an important parameter of male reproductive success. However, since the intensity of breeding colour was positively correlated with aggressive behaviour, it is difficult to determine whether the enhancement of male reproductive success was caused by nuptial colour per se or associated courtship and aggressive behaviour. The lack of correlation between male aggressiveness and reproductive success (Table III) is surprising, and reinforces the conclusion that the important criterion of female choice of a male's personal characteristics is his nuptial colour. However, the incitation hypothesis (Cox & Le Boeuf 1977) cannot be ruled out, because females often enter several territories in succession and this

136

ANIMAL

BEHAVIOUR,

results in fights between n e i g h b o u r i n g males ( K o d r i c - B r o w n , u n p u b l i s h e d data). Size of males did n o t e n h a n c e reproductive success p r o b a b l y because o f the intense intramale competition, that resulted in a close m a t c h in competitive ability. Personal characteristics o f a male m a y n o t only enhance the survival of the eggs, b u t also c o n t r i b u t e to the genetic fitness of b o t h male a n d female offspring. Females could select males o f high genetic quality if there is a correlation between male genotype a n d phenotype. Wide v a r i a t i o n in the intensity of b o t h n u p t i a l colorat i o n a n d agonistic b e h a v i o u r within a n d between individual males suggests that these male charac, teristics most likely have low heritability a n d c a n be only indirect indicators o f genetic quality. Nevertheless they appear to be accurate indicators o f males' physiological a n d m o t i v a t i o n a l state. Males that sustain high levels of n u p t i a l coloration are aggressive a n d successful in o b t a i n i n g a n d m a i n t a i n i n g a territory of high quality in a highly competitive e n v i r o n m e n t . These males are consistently chosen by females a n d enjoy a high reproductive success. AeknoMedgments I a m grateful to Renee Vestal a n d Jerry N a t h a n for their help in the field, a n d to M a t h e w Leibold a n d L a u r a Key for assistance with the statistical analysis. James H. Brown provided helpful c o m m e n t s o n the manuscript. The research was supported by the N a t i o n a l Science F o u n d a t i o n G r a n t (DEB 7905846).

REFERENCES

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'sexy son' hypothesis revisited. Am. Nat., 117, 329-342. (Received 5 February 1982; revised 10 May 1982; MS. number: A2796)