Behavioral Ecology Advance Access originally published online on June 11, 2004
Behavioral Ecology 2004 15(5):872-882; doi:10.1093/beheco/arh100
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Intrasexual selection and group spawning in quacking frogs (Crinia georgiana)
School of Animal Biology M092, University of Western Australia, 35 Sterling Highway, Crawley, WA 6009, Australia
Address correspondence to P. G. Byrne, who is now at the Division of Botany and Zoology, The Australian National University, Canberra, ALT 0200, Australia. E-mail: phillip.byrne{at}anu.edu.au.
Received 5 June 2003; revised 30 January 2004; accepted 13 February 2004.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
In the Australian frog Crinia georgiana, matings frequently involve a single female and multiple males (group spawning). The aim of the present study was to demonstrate a connection between variation in the intensity of intrasexual competition, measured by using male density and operational sex ratio (OSR), and the incidence of group spawning. Over a 3-month breeding period, male density and OSR varied substantially and were significantly influenced by climatic conditions. The frequency of agonistic interactions between males was higher in denser choruses. Fights were typically over the possession of sites used to broadcast advertisement calls and were almost always won by larger males. At higher densities, males allocated significantly less time to calling to attract females and spent more time as nonmoving satellites or roaming through an aggregation (searching). However, large males always called more than did small males. The number of males involved in a spawning correlated positively with variation in both male density and OSR. Observation of group spawnings revealed that they generally arose when a satellite male joined a mating pair after a female chose to mate with a calling male or when a female was seized by a searching male and the pair was joined by other searching males. These findings, coupled with past research documenting costs but no benefits of multiple paternity to females, suggest that competitively inferior males force group spawns.
Key words: forced copulation, frogs, group spawning, sexual conflict.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Disparity in mating interests between the sexes conventionally arises because males have a higher potential reproductive rate than do females. Consequently, females exert mate choice (intersexual selection), whereas males have to compete for matings (intrasexual selection; Andersson, 1994
; Trivers, 1972). These sexual differences are reflected in the operational sex ratio (OSR); the ratio of fertilizable females to sexually active males at the site and time when mating occurs (Emlen and Oring, 1977). The OSR provides a useful empirical tool for measuring and predicting the intensity of intrasexual selection. With an increasing bias in the OSR toward males, increased competition for females is expected (Kvarnemo and Ahnesjö, 1996). The density of breeding males may also influence the intensity of intrasexual competition (Conner, 1989). As the distance between competing individuals decreases, often owing to clumped distribution of resources, the encounter rate, and hence frequency of agonistic interactions, between males is likely to rise (de Boer, 1981). Because changes in male density can alter the ratio of males to females at a breeding site, they may also have important effects upon the OSR. There is empirical support for the use of both OSR and density as measures of the intensity of intrasexual selection (de Boer, 1981; Gwynne, 1984; Madsen and Shine, 1993).
Under conditions of intense intrasexual selection, large variance in male-mating success is expected (Andersson, 1994). In such situations there will be strong selection pressure on unattractive and subordinate males to adopt alternative mating tactics (Gross, 1996). Occasionally males mimic females to obtain matings. This is usually a sophisticated tactic, which requires marked behavioral or morphological changes (Thornhill, 1979). Subordinate males may also gain matings by closely attending displaying males and intercepting females as they approach. This behavior, termed satelliting, occurs in many taxa (Cade, 1979; Sullivan, 1982; Widemo, 1998). However, the most widespread alternative tactic is sneaking, in which a male steals fertilizations from a male already paired with a female (Taborsky, 1998). Sneaking may be a conditional strategy (Simmons et al., 1999), may be a genetically fixed strategy (Zimmerer and Kallman, 1989), or be used opportunistically (Austad, 1984).
Among anuran amphibians, there is considerable variation in mating system structure arising from variation in the intensity of intrasexual selection related to the length of the breeding season (for review, see Sullivan et al., 1995). Wells (1977) described anurans with short breeding periods lasting hours to days as explosive, contrasting them with prolonged breeders who breed over periods of weeks to months. In explosive breeders, female choice is temporally constrained, and the synchronous arrival of the sexes to a breeding site limits the possible skew in male-mating success. When breeding is prolonged, females have more time to choose a mate, but males can usually mate many times over a season so there are increased opportunities for mate monopolization (Sullivan et al., 1995).
In anurans with both explosive and prolonged breeding, males generally gather at sites where females prefer to lay their eggs and use an advertisement call to attract a mate (Sullivan et al., 1995). However, within an aggregation of calling males, termed a chorus, acoustic competition is often intense and only males that invest heavily in calling, for example, by increasing call rate or duration, are likely to attract females (see Halliday and Tejedo, 1995; Smith and Roberts 2003a). Consequently, when competition becomes too intense, males often abandon calling for alternative noncalling mating tactics. In many explosive breeding species, males call to attract females at low male density, but when male density becomes too high, they resort to actively searching a breeding area for females (scramble competition; see Halliday and Tejedo, 1995). In prolonged breeders the alternative to calling is usually to act as a satellite (Lucas et al., 1996). In some species, noncalling males may simply be waiting for call sites to become available (e.g., Hyla versicolor; Fellers, 1979). Alternatively, calling and satellite behavior may represent a mixed evolutionary stable strategy (ESS) in which both strategies yield equal mating success (e.g., Hyla cinerea; Perril et al., 1982). For most species, however, silent males are inferior acoustic or physical competitors that are making the "best of a bad lot" by intercepting females that are attracted to callers (see Halliday and Tejedo, 1995).
Inferior male anurans may also improve their reproductive success by joining mating pairs and sneaking fertilizations. In at least 10 species from three families, it has been reported that spawnings can involve single females and multiple males (group spawning; Halliday, 1998). In many of these taxa, competition between males for mates is intense, and group spawning has been interpreted as a strategy used by males to secure fertilizations without having attracted a female through advertisement (D'Orgeix and Turner, 1995; Fukuyama, 1991; Jennions et al., 1992; Jennions and Passmore, 1993; Kusano et al., 1991; Pyburn, 1970; Roberts, 1994). However, for most of these anuran species, a detailed understanding of the adaptive significance of group spawning is lacking. Consequently, a direct connection between the intensity of intrasexual selection and group spawning in anurans remains to be demonstrated.
In the Australian myobatrachid frog, Crinia georgiana, group spawning occurs in approximately 50% of matings and results in multiple paternity of egg clutches (Roberts et al., 1999). On average, females are amplexed (sexually embraced by a male) by two males, but up to nine males may become involved. This mating pattern entails extreme reproductive costs to females because interactions between competing males lead to reduced fertilization success and sometimes mortality (Byrne and Roberts, 1999). Moreover, laboratory experiments provide no evidence that the immediate fitness costs incurred by females are compensated by increased genetic quality of her offspring, leading to increased numbers of grand-offspring (Byrne and Roberts, 2000), an indirect benefit of multiple paternity found in some polyandrous insects, arachnids, birds and mammals (cf. Jennions and Petrie, 2000; Stockley et al., 1993; Yasui, 1998).
Within breeding aggregations male densities are frequently high and the OSR is usually heavily male biased (Byrne and Roberts, 2000). It has also been observed that fights between males are common and that a proportion of males within a chorus do not call but either remain motionless in close association with a caller or roam the breeding area (Byrne, 2002b). Based on these observations, we predict that group spawnings occur in Crinia georgiana because intense intrasexual competition forces competitively inferior males to gain fertilizations by joining mating pairs. Specifically, we argue that (1) variation in OSR and male density over a breeding season is substantial and correlates with climatic variables; (2) variation in male density affects the frequency of agonistic interactions between males; (3) variation in male density, coupled with male body mass, affects whether males call to attract females or adopt noncalling mating tactics; (4) variation in male density and OSR influence the number of males involved in a spawn; and (5) group spawns are the outcome of competitively inferior noncalling males joining mating pairs. These predictions are based on the assumption that variation in OSR and male density are correlated with variation in the intensity of intrasexual selection.
The results of the present study will have significant implications for anuran breeding biology and sexual selection theory for two main reasons. First, they will provide an insight into the evolution of group spawning, a mating system that may be widespread amongst anurans yet remains largely uninvestigated (cf. Byrne et al., 2002, 2003; Halliday, 1998). Second, they will contribute to our current understanding of why females mate with multiple males, a topic that remains one of the most compelling questions in evolutionary biology.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Study species
Crinia georgiana is a small frog (snout-vent length = 18–47 mm; Smith and Roberts, 2003b
) that is abundant and widely distributed throughout southwestern Australia. Breeding takes place at night between midautumn and late spring. Males aggregate in sparsely vegetated areas covered by shallow water (approximately 5–10 mm deep) and call to attact females (Main, 1965). Within the chorus of calling males, individual males physically defend depressions in the substrate that function as stations for broadcasting the advertisement call. However, these call stations are usually only defended for a few nights because they either become flooded after heavy rainfall or they dry out between rain events (Byrne, 2002b). Individual females are attracted to the vocalizations of a specific male (Smith and Roberts, 2003a) and typically initiate amplexus (sexual embrace of a female by a male) by moving under a caller between the arms or along the side between the arms and legs (Byrne, 2002b). During single-male matings (pair spawnings), males mount females dorsally and embrace them in front of the hind legs (inguinal amplexus), indicating this is the preferred (focal) amplectant position. During group spawnings (two or more males with one female), second males typically clasp the female ventrally, and additional males clasp the female dorsolaterally (for illustration, see Roberts et al., 1999). Eggs are shed into shallow water and fertilized externally as they are released. The eggs are large and generally deposited in discrete clumps at the site where a male advertises (Byrne, 2002b; Seymour and Roberts, 1995). Paternity analysis of egg clutches deposited during group spawnings indicates that males in the dorsal and the ventral positions both gain a share of paternity but other males do not (Roberts et al., 1999).
Study site
The investigation was conducted in a natural breeding population near Kangaroo Gully 30 km southeast of Perth, Western Australia. The 600-m2 study site was a series of shallow seasonal pools that formed on a sloping, moss-covered, granite outcrop surrounded by low scrub and forest. Throughout the breeding season, males aggregated at different locations within this site, depending on the distribution of shallow water. Because of the open nature of the study site individual frogs were easily observed. Data were collected on 44 nights between 1700 and 0500 h from 12 June to 27 August 1998.
Detection of spawning frogs and measurement of OSR and male density
Spawning frogs were located by using an infrared NAV 3 night vision scope to search through the chorus. When encountered, a 1-m2 quadrat was placed over the frogs and arranged so that the pair or group was situated centrally. Because the study site was an open area and the frogs only breed in shallow pools, it was easy to locate mating frogs irrespective of whether they were in a pair spawning or in a group spawning. Therefore, we are confident that there was no sampling bias. For each spawning the number of males and females within the quadrat were counted. Because females left a chorus after egg deposition, most females encountered were gravid (clearly evident from their bellies being distended with eggs). On the rare occasion that nongravid females were encountered, they were deemed sexually inactive and excluded from counts. Because the number of frogs present around a mating could change with the movement of females and males through the chorus, it was necessary to make counts quickly. Preliminary investigation confirmed that the number of frogs present in an area of 1 m2 could be accurately and efficiently counted, but that counts made in quadrats of greater size were prone to error. This was the justification for using 1 m2 as the sample area. OSR was calculated as the number males not physically grasping a female/[(number gravid females not grasped by a male) + (number of males not grasping a female)] (Emlen and Oring, 1977) and male density as the total number of males not grasping a female in the quadrat. In this way the central mating pair/group was excluded from our measures. For 13/101 spawns encountered, there was a second mating pair/group present in a quadrat. These frogs were excluded from the estimate of OSR and male density because we considered that the females were no longer fertilizable and that the males were sexually preoccupied (Emlen and Oring, 1977). When two matings were encountered at the same time, we focused on the mating in which the female was in the earliest stage of egg deposition. In this way the estimate of OSR and male density was made close to the time when spawning commenced.
Seasonal variation in male density and OSR
We used one-way ANOVA's to test whether male density and OSR varied significantly between nights censused over the breeding season. In addition, we used simple-regression analysis to determine whether male density and OSR increased or decreased with time (days) since the beginning of the breeding season.
Effect of climate on variation in male density, female chorus attendance, and OSR
We calculated the relationships among male density, number of females encountered in a chorus, OSR (dependent variables), and three climatic variables (rainfall, lunar phase, and temperature) by using multiple-regression models. Rainfall and lunar phase were considered because previous work indicates that breeding activity in C. georgiana is influenced by these two variables (Byrne, 2002a). Temperature was also tested because the activity of ectotherms is often temperature dependent (Kvarnemo et al., 1995). Sampling involved randomly searching choruses for females (see above). Searches commenced between 1800 and 1930 h and finished no later than 0500 h. Searches were abandoned if no females were detected after 90 min. When females were detected, measures of OSR and male density were made after they amplexed (see above). On nights in which no females were present, OSR was not estimated, but male density was estimated by randomly placing a 1-m2 quadrat in the chorus and counting the number of males within it. For every nightly census, a minimum of three and a maximum of 21 quadrats were sampled. Information on daily rainfall was acquired from a recording station located approximately 8 km southwest of the study site. Information on lunar cycle was acquired from the Perth Observatory. Variation in temperature was recorded on site by using an HDL data logger. Estimates of nightly temperature were made by averaging seven recordings taken at 2-hour intervals between 1800 and 0600 h. For analyses, average nightly male density, total number of females encountered per night, and average nightly OSR were the dependent variables and mean nightly temperature (in Celcius), days since rain (more than 3 mm), and days since full moon were the independent variables.
Effect of male density and temperature on the frequency of male-male competition
To determine the effect of male density on the frequency of physical interactions between males, 18 aggregations of males, all from separate nights, were video-recorded under infrared light by using a Canon UC V1000 camcorder with Nav 3 Night Vision attachment. Recording periods lasted from 5–10 min. After each recording, male density was determined within the area monitored by randomly placing a 1-m2 quadrat in the aggregation and counting the number of males within it. This was repeated six times and an average taken. Because the intrasexual behavior of ectotherms may be influenced by temperature (Kvarnemo et al., 1995), water temperature was also measured by using a Miller and Weber thermometer. From videos we used dorsal patterns and body size to identify individual males and counted the number of interactions per male (cf. Gerhardt et al., 2000; Main, 1965; Roberts et al., 1999; Smith and Roberts, 2003a,b). Duration of observations were timed (to the nearest second) by using a stopwatch. A total of 140 males were observed. The influence of density and temperature on number of interactions per male was determined by using multiple regression. For this analysis, both the number of interactions per male per minute and male density were log transformed (common log). We also observed the events that led to 47 physical contests between males. Precombat behavior of males was assigned to one of four categories: (1) calling from a set site in the chorus, (2) calling and moving through the chorus, (3) silent and stationary in the chorus, or (4) silent and moving through the chorus. A Fisher's Exact test tested for significant differences in the proportion of fights that arose from competition over call sites (versus those that were not call site related) at low male density (less than five males per meter squared) and high male density (more than five males per meter squared). This density division was chosen because five males per meter squared was approximately the average density of males within a chorus for nights where breeding activity occurred (see Results). When physical interactions occurred between males, the duration that males remained in contact with each other was timed (to the nearest second) using a stopwatch. After interaction, males were collected and weighed (to the nearest 0.1 g) by using a digital balance. Simple-regression analysis was used to determine whether difference in body mass between contestants (mass of largest male minus mass of smallest male) effected the duration of interaction. For analysis, difference in body mass was the independent variable and duration of interaction in seconds was the dependent variable. When interactions were resolved, victory was assigned to the male that remained at the site of initial contact.
Effect of male density and body mass on male-mating behavior
From video recordings, we calculated time spent by 54 males in three behaviors: (1) calling (advertising), (2) stationary and silent (satelliting), and (3) silent and moving (searching). Behavioral analyses commenced when a female entered into a group of calling males within the chorus and were terminated when males attempted to grasp or successfully amplexed the female. In this way all observations were standardized to the period that a female was present. The influence of male density and body mass on the preamplectant behavior of males was determined by using multiple-regression analysis with male density and body mass as independent variables, and the difference between the time males spent calling and the time males spent silent (silent motionless + silent and moving) as the dependent variable. For analysis, behavioral durations were log transformed (common log).
Effect of OSR and male density on the number of males involved in a spawning
The number of males involved in 101 spawns was recorded in addition to measures of male density and OSR (defined above). To test the hypothesis that the incidence of group spawning is related to variation in the intensity of intrasexual competition, we determined whether the number of males involved in a spawning was dependent on male density and/or OSR at the mating site at the time mating occurred. This was done by using two separate simple-regression analyses with either OSR or male density as the independent variable and the number of males involved in a spawning as the dependent variable.
Effect of male density and body mass on the amplectant position obtained by males involved in group spawnings
Assuming that group spawnings arise owing to competitively inferior (presumably smaller) males forcing copulation, we predicted that smaller males will normally be in ventral (nonpreferred) amplexus positions. If male density affects male-mating behavior (see above), we also predicted that any relations evident between body mass and amplectant position will differ under conditions of low versus high male density. For 52 group spawnings, frogs were collected after the completion of egg deposition and weighed (to the nearest 0.1 g) by using a digital balance. Matings were scored as occurring at low or high male density (defined above). For spawns occurring in each male density category (low or high), one-way ANOVA was used to test the association between amplectant position (focal, ventral, dorsolateral) and male body mass. Post hoc comparisons were made by using Scheffe F tests.
Formation of pair and group spawnings
To test the hypothesis that group spawnings are the outcome of noncalling (satellite or searching) males joining mating pairs, females were detected by randomly traversing the study site. They were then followed until they mated (observed as above). A minimum distance of 1.5 m was kept from females at all times to minimize disturbance. Frogs only became visibly disturbed when observations were made at a distance of less than half a meter. A total of 59 matings were observed. Of these 24 were video recorded. The behavior of males that became involved in matings was recorded and assigned to one of four categories: (1) calling from a set site in the chorus (advertising), (2) calling and moving through the chorus (advertising and searching), (3) silent and stationary in the chorus (satelliting), or (4) silent and moving through the chorus (searching). We also recorded whether spawnings originated because females chose males, female initiated contact with a male by moving under him, or males forced copulation by intercepting females. Binomial tests were used to determine whether the proportion of pair and group spawnings occurring on low-density nights (42% of nights surveyed) versus high-density nights (38% of nights surveyed) were significantly different. For both pair and group spawnings, Fisher's Exact tests were used to determine whether (1) there were significant differences in the proportions of calling versus noncalling males involved in spawns that occurred at low and high male density (defined above), and (2) whether there were significant differences in whether spawns resulted from choice or were forced at low and high male density.
Data analysis
All analyses were made using either JMP or Statview statistical software packages. The significance level used was a = 0.05. For multiple-regression analyses, partial correlation coefficients were obtained by using a correlation coefficient matrix.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Seasonal variation in male density and OSR
The mean density of males in a nightly chorus was approximately 4 m–2 (3.67 ± 0.29 [SE], n = 138 samples). On nights on which females were present in the chorus (n = 21), the average density of males was approximately 5 m–2 (5.05 ± 0.36, n = 91 samples). Male density varied significantly between nights, ranging from one male to 18 males/m–2 (one-way ANOVA F43,137 = 4.30, p = <.001) (Figure 1). Male density did not vary predictably with time since the beginning of the breeding season (simple regression r 2 =.06, F1,43 = 2.70, p =.10).
|
The mean OSR was male biased (0.76 ± 0.01, n = 92 samples). OSR varied significantly between nights that females were present in the chorus (n = 21), ranging from even (0.5) to heavily male biased (0.94; one-way ANOVA F20,91 = 6.06, p = <.001) (Figure 2). Mean nightly OSR did not vary predictably with time since the beginning of the breeding season (simple regression r 2 = <.03, F1,20 = 0.64, p =.43).
|
Effect of climate on variation in male density, female chorus attendance, and OSR
Climatic conditions significantly influenced male density (multiple regression r 2 =.425, F3,43 = 9.84, p <.01). Number of days since full moon and the number of days since rainfall were negatively correlated with male density, whereas air temperature was positively correlated with male density (lunar phase: partial corr. coefficient = –0.53, t = 4.0, p <.01; rainfall: partial corr. coefficient = –0.43, t = 3.0, p <.05; temperature: partial corr. coefficient = 0.37, t = 2.5, p <.05).
The number of females detected in a chorus was also significantly influenced by climatic conditions (multiple-regression analysis: r2 =.26, F3,43 = 4.85, p <.01). Lunar phase and rainfall were significantly negatively correlated with the number of females detected (lunar phase: partial corr. coef. = –0.44, t = 3.1, p <.01; rainfall: partial corr. coef = –0.35, t = 2.4, p <.05), but air temperature did not make a significant contribution to the model (temperature: partial corr. coef = 0.04, t = 0.26, p >.05).
Climatic conditions also significantly influenced the degree of male bias in the OSR (multiple regression: r2 = 0.42, F3,20 = 4.13, p =.02). However, only days since rainfall made a significant contribution to the model (rainfall: partial corr. coef = –0.49, t = 2.3, p <.05; lunar phase: partial corr. coef. = –0.29, t =1.2, p >.05; temperature: partial corr. coef = 0.39, t = 1.8, p >.05).
Effect of male density and temperature on the frequency of male-male competition
Male density and water temperature independently explained a significant proportion of the variation in the frequencyof agonistic interactions between males (multiple regression: r 2 = 0.36, F2,139 = 38.1, p <.001). Both variables were positively correlated with the frequency of agonistic interactions (male density: partial corr. coeff. = 0.58, t = 8.3, p = <.001; water temperature: partial corr. coeff. = 0.27, t = 3.4, p <.001).
Most male-male interactions, (29/47, 61.7%) occurred owing to disputes over water filled depressions used by males as call sites (see Appendix). These fights arose either because (1) calling males attacked males which began calling in close proximity, (2) calling males attacked silent males positioned in close proximity, or (3) silent males moving through the chorus attacked males that were calling from fixed sites. Interactions that were not over call sites arose when males attempted to amplex other males (13/47, 27.6%) or males inadvertently contacted other males while moving through the chorus (5/47, 10.6%). The proportion of fights arising from competition over call sites versus those that were not call site related, at low versus high male density, were significantly different (low male density; call site related = 24/27, high male density; call site related = 5/20, Fisher's Exact test: n = 47 male-male interactions, p = <.0001).
|
Effect of male body mass on success in male-male competition
Success in combat was size dependent. With one exception (one out of 47 contests), larger contestants were always victorious (see Appendix). Interactions between males lasted from 2–180 s (mean = 49.3 ± 9.1, n = 31). As the difference in body size between males increased, the duration of an interaction decreased (simple-regression: r 2 = 0.17, F1,30 = 5.99, t = –2.45, p =.02). Data regarding the body mass of males involved in combat, differences in mass between contestants, precombat behavior of contestants, and duration of interaction are presented in Appendix.
Effect of male density and body mass on male-mating behavior
Time spent by preamplectant males calling versus silent was significantly effected by both body mass and male density (multiple regression: r 2 = 0.22, F2,53= 7.56, p =.0013). Male density had a significant negative effect upon duration males spent calling relative to duration spent silent (coeff = –6.20 ± 2.32, t = 2.68, p =.01), whereas body mass had a significant positive effect upon duration males spent calling relative to duration spent silent (coeff = 11.85 ± 3.63, t = 3.26, p =.002).
Effects of variation in density and OSR on the number of males involved in spawns
The number of males involved in a spawning averaged 1.94 (±0.09, n = 101 matings), but ranged between one and seven (Figure 3). Male density had a significant strong positive influence on the number of males involved in a spawning (simple regression: r 2 =.44, F1,90 = 69.29, p <.0001) (Figure 4a), as did the degree of male bias in the OSR (simple regression: OSR: r 2 =.44, F1,90 = 68.14, p <.0001) (Figure 4b).
|
|
Effect of density and body mass on the amplectant position of males involved in group spawnings
For group spawnings that occurred at densities of five males per meter squared or less (n = 26), the body mass of males was significantly associated with amplectant position (one-way ANOVA F 2,56 = 23.89, p = <.0001). Males amplexing dorsally were significantly larger than were males amplexing ventrally (Scheffe F test = 22.50, p <.05) or in any other position (Scheffe F test = 6.15, p <.05) but males amplexing in nondorsal positions (ventral or dorsolateral) did not differ significantly in body mass (Scheffe F test = 0.46, p >.05) (Figure 5a). For group spawnings that occurred at densities greater than five males per meter squared (n = 25), the body mass of males was not significantly associated with amplectant position (one-way ANOVA: F2,81 = 0.54, p =.58) (Figure 5b).
|
Observation of the formation of pair and group spawnings
Seventeen out of 22 pair spawnings observed occurred at low male density, which was significantly more than expected (p <.001). Of these, most resulted from a female initiating amplexus with a calling male. Of the five pair spawnings observed under conditions of high male density, most resulted from a female being intercepted by a noncalling searching male (Table 1). The proportion of spawns that involved calling versus noncalling males at low versus high male density was significantly different (low male density: calling = 14/17; high male density: calling = 1/5, Fisher's Exact test: n = 22 pair spawnings, p =.02). The proportion of spawnings arising from female choice versus male interception at low versus high male density was also significantly different (low male density: choice = 13/17; high male density: choice = 1/5, Fisher's Exact test: n = 22 pair spawnings, p =.03).
|
Out of 37 group spawnings observed, 18 occurred at low male density and 19 at high male density. These ratios were not significantly different than expected (p =.24). Under conditions of low male density, group spawnings were largely the outcome of a female initiating mating with a calling male and the resultant pair being joined by a satellite male (Table 2). Under conditions of high male density, group spawnings usually arose when a female was intercepted by a calling or noncalling searching male and the resultant pair was joined by one or more searching noncalling males and/ or searching calling males (Table 2). The proportion of males involved in spawnings that were calling versus noncalling, at low versus high male density, was not significantly different (low male density: calling = 20/42; high male density: calling = 22/55, Fisher's Exact test: n = 97 males, p =.53). However, the proportion of group spawnings arising from female choice versus male interception at low versus high male density was significantly different (low male density: choice = 13/18, high male density; choice = 6/19, Fisher's Exact test: n = 37 group spawnings, p =.02).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Seasonal variation in male density and OSR
In the Australian frog C. georgiana, the density of males and the number of females detected in a chorus varied greatly over the course of a breeding season. A significant amount of this variation was explained by rainfall and lunar phase, suggesting that the sexual activity of both sexes is synchronized by these climatic variables. Not surprisingly, these findings agree with an earlier study that found that the number of matings detected at a breeding site was influenced by the same climatic variables (Byrne, 2002a
). They also agree with studies for other frogs that have shown reproductive activity is stimulated by climatic variables (Bush, 1993; Church, 1960a,b; Sinsch, 1988). The effect of rainfall is likely to be directly related to the fact that spawning takes place in temporary pools that form after rain (Ayre et al., 1984; Main, 1965). The adaptive benefit to both sexes of attending the chorus closer to a full moon may be related to visual cues being important in mate choice (Duellman and Trueb, 1986) or because increased light availability aids in predator detection and evasion (Tuttle and Ryan, 1982; Tuttle et al., 1982). For females, the lunar cycle could also play a role in regulating ovulation (Church, 1960a,b). Variance in male density and female chorus attendance that remained unexplained by climate may relate to fluctuations in the abundance and distribution of resources required for breeding (e.g., call sites and oviposition sites; cf. Donnelly, 1989; Pröhl, 2002; Stewart and Pough, 1983), migration of frogs to and from nearby choruses (Murphy, 1994), or intrinsic factors that determine when breeding condition is reached, for instance, the age at maturity and the level of stored energy available (Halliday and Tejedo, 1995; Kvarnemo, 1997; Kvarnemo and Simmons, 1999; Murphy, 1994).
The ratio of males to females (OSR) in the chorus varied considerably over the breeding season, ranging from even to heavily male biased. A significant portion of this variation can be explained because the OSR became less male biased with increasing time since rainfall. Given that OSR is a function of the number of males and females present within the chorus, this relationship probably occurred owing to the negative effect that increasing time since rainfall had on both male density and female chorus attendance. However, because most of the variation in OSR was unexplained, OSR must be sensitive to variables other than climate. These are probably diverse but may include variation in the social environment such as the quality and distribution of males within the chorus (Kokko and Johnstone, 2002; Otronen, 1996) or variation in the physical environment such as the quality and distribution of resources necessary for female reproduction (e.g., tadpole rearing sites; Pröhl, 2002).
Male-male competition, male mate-acquisition behavior, and group spawning
Changes in male density and OSR have an important influence upon the intensity of intrasexual competition, male-mating tactics, and the incidence of group spawning. Consistent with our predictions, males fought more at higher densities (Andersson, 1994) and higher temperatures (Kvarnemo et al., 1995). At low male density, most fights were over the possession of water filled depressions used as call stations. This finding suggests that call stations are a scare resource and that, at low male density, advertising is an important determinant of male-mating success. However, because female C. georgiana deposit their eggs at the site where a male is advertising, males may also be defending oviposition sites that are preferred by females. Resource defense mating systems have been reported in several frog groups, including North American ranids (Howard, 1978a,b; Wells, 1977), neotropical dentrobatids (Summers, 1992a,b), and a hylid from Central America (Kluge, 1981). At high male density, fights were generally instigated when males roaming the chorus inadvertently contacted, or attempted to amplex, other roaming males. This suggests that males abandon the defense of call sites, or oviposition sites, at high male density. Density-dependent switches in male-mate acquisition behavior are common in anurans (see Discussion below). Almost invariably large males were competitively superior in physical interactions: a common result in anurans (see Davies and Halliday, 1979; Halliday and Tejedo, 1995).
Variation in male density, and male body mass, also correlated with variation in the reproductive behavior of males. With increasing male density, males allocated less time to calling and more time to satellite behavior or roaming (searching) the chorus. Large males allocated significantly more time to calling than did small males. Small males may allocate less time to calling because they are energetically constrained. In some frogs males switch from calling to less costly silent behavior when their energy reserves become depleted (Arak, 1988). It is also possible that small males avoid calling because their calls are less attractive to females, either because females have a sensory bias for size-related call characteristics (Gerhardt, 1994; but see Smith and Roberts, 2003a where high call rates are attractive and smaller males call faster) or because there are direct or indirect benefits to females of selecting large sires (Doty and Welch, 2001; Mitchel, 1990; Woodward, 1986, 1987). However, manipulative field experiments in C. georgiana have shown that when calling males are removed from a chorus, noncalling males quickly locate unoccupied call sites and commence advertising (Byrne, 2002b). This implies that calling is the preferred tactic, a conjecture supported by the finding that most pair spawnings arose when a female chose to mate with a calling male. Therefore, it seems that male reproductive behavior is probably conditional on body mass because large males win fights and monopolize call space. Small, competitively inferior males are then probably forced to adopt alternative noncalling tactics to obtain matings. This relationship is likely to be accentuated with increasing male density when call space becomes increasingly limited.
At low male density, noncalling males sometimes secured mates by closely associating with a calling male and intercepting females that approached. This "satellite behavior" has been widely reported as an effective condition-dependent alternative mating tactic used by small male anurans (Arak, 1988; Howard, 1978a; Krupa, 1989; Perrill et al., 1978). With increasing male density, all males, irrespective of body size, allocated less time to calling and more time to remaining silent and motionless in the chorus or silently roaming the chorus. This explains the finding that, at high male density, only a small proportion of pair spawnings were the outcome of females choosing a calling male. Conversely, the majority of pair spawnings that occurred at high male density arose when noncalling males that had been searching the chorus seized (intercepted) females. This mating pattern resembles that of explosively breeding anurans in which males call to attract females at low male density, but in dense aggregations, alternate between calling and competing directly by searching for females (Halliday and Tejedo, 1995). Species from the genus Bufo (e.g., Bufo bufo, B. calamita, B. woodhousii, and B. valliceps) are renowned for their high plasticity in competition behavior depending on male density (see Arak, 1983; Höglund and Robertson, 1988; Sullivan, 1989; Wagner and Sullivan, 1992). Density-dependent expression of calling and searching behavior is also well documented for Rana sylvatica (Woolbright et al., 1990) and R. catesbiana (Emlen, 1976; Howard, 1978a).
As predicted, a connection was evident between variation in the intensity of intrasexual competition and the occurrence of group spawning. Variation in both male density and the degree of male bias in the OSR strongly correlated with the number of males involved in a spawning. At low male density, group spawnings generally arose when a satellite male joined a mating pair after a female chose to mate with a calling male. Given that calling males are usually of larger body mass, this explains the finding that males amplexed in the dorsal (preferred) position were significantly larger than were males amplexed in ventral or dorsolateral positions. At high male density, group spawns generally arose when a searching male seized a female and other searching males joined the pair. Under these conditions, there was no relationship evident between male body mass and amplectant position. Within the pool of larger males using noncalling tactics at high male density, there is no large male advantage in the scramble to intercept females; a pattern also reported in common toads (Höglund and Robertson, 1988). We conclude that competitively inferior males, which are unable to secure call sites to attract mates at low male density or secure mates directly during scramble competition at high male density, force group spawnings.
Males may not make a discrete decision to adopt a specific mating tactic but switch between them opportunistically, depending on their competitive status and the frequency of physical interaction. Satelliting, searching, and joining mating pairs may simply be three different expressions of males making the best of a bad lot. Interceptions may be made if females are detected in close proximity, but if these opportunities do not arise, unsuccessful males may settle for joining pairs and gaining a share of paternity (see Roberts et al., 1999). However, because considerable precision is required to secure a passing female and failed grasping attempts often evoke a flight response (Byrne, 2002 b), waiting for pairs to join may provide more predictable returns. When the OSR is even or slightly male biased, failed interceptions may not greatly affect individual fitness because the probability of encountering other females is high. But considering that OSR in C. georgiana is normally moderately male biased, any missed matings owing to failed interception may be extremely costly. Once a female is clasped by a male, ventral amplexus is easily obtained by secondary males and guarantees a significant proportion of fertilizations (Roberts et al., 1999). This may strongly favor males that join mating pairs.
The strategy of joining mating pairs used by inferior males is comparable to sneaky matings in fish in which subordinate males parasitize the reproductive success of territorial males by swimming between spawning pairs and releasing sperm (Gross, 1982). In fish, Taborsky (1998) found that simultaneous parasitic spawning is evident in 140 species from 28 families. Among anuran amphibians, C. georgiana provides the only example in which sneaking appears to be a specialized male strategy to compensate for competitive inferiority owing to pheneotypic constraint, although it has been suggested that secondary males may be using sneak tactics in several other anurans that exhibit group spawning. These include foam nesting Rhacophorids (Fukuyama, 1991; Jennions and Passmore, 1993; Jennions et al., 1992; Kusano et al., 1991), leaf-frogs (Pyburn, 1970), red-eyed tree frogs (D'Orgeix and Turner, 1995), and explosive breeding neo-tropical frogs (Roberts, 1994). However, in these species males that join pairs do not differ phenotypically from paired males, suggesting that all males use this tactic opportunistically (Halliday, 1998). Thorough investigation of the behavior of joining pairs in other anurans is now required to unravel the forces generating its expression.
Given that group spawnings in C. georgiana entail extreme costs to females (Byrne and Roberts, 1999) and provide no apparent compensatory genetic benefits (Byrne and Roberts, 2000), this mating pattern appears to occur against the reproductive interest of females and provide another example of forced copulation by males (Constanz, 1975; Kodric-Brown, 1977; McKinney et al., 1983; Severinghaus et al., 1981; Thornhill, 1980; Westneat, 1987). If this is the case why do females not actively fight to break away from matings involving multiple males? Within choruses it has been observed that males are attracted to movement (Byrne, 2002b). By struggling to repel unwanted males, females may attract further males and entail increased costs. Consequently, females may accept matings out of convenience (Rowe, 1992). Alternatively, resistance may be futile. In many species females succumb to male harassment because resistance is ineffective (Clutton-Brock and Parker, 1995). A general pattern among anurans is that females are larger than are males (Shine, 1979). A lack of size dimorphism in C. georgiana (Smith and Roberts, 2003b) may make rejection of mating attempts difficult, particularly when several males are involved. Moreover, males possess huge forearms relative to their body size (Byrne, 2002b). The absence of this trait in other members of the genus suggests it has probably evolved to aid males in securing females under conditions of intense intrasexual competition. Among anurans that compete directly for females, increased forelimb size is common and has been attributed to providing males with increased ability to secure females and/or resist displacement from amplexus by rival males (cf. Bourne, 1992; Howard and Kluge, 1985). Adaptive traits to procure females have also been reported for other taxa in which males compete vigorously for females. For example, in water striders males force females to mate by grasping them with abdominal claspers (Arnqvist and Rowe, 1995).
How often group spawning in anurans is driven by intrasexual selection as opposed to female benefit remains an unresolved question. Worldwide, group spawning in anurans has been reported in approximately 10 species from three different families (Halliday, 1998). However, cost/benefit analyses for these groups are lacking. Experimental investigation of group spawning in other anurans is now required to establish the general applicability of forced copulation as an explanation for the evolution of group spawning in anuran amphibians.
|
ACKNOWLEDGEMENTS |
|---|
Many thanks to Leigh Simmons, Tim Halliday, Geoff Parker, Mathew Gage, Michael Jennions, and two anonymous reviewers for comments on the manuscript. Research was supported by a Gene Rodgerson Scholarship and the Australian Research Council. Research was conducted with permission of the Animal Ethics and Experimentation Committee (U.W.A.; approval no. 117/97).
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Arak A, 1983. Male-male competition and mate choice in anuran amphibians. In: Mate choice (Bateson PPG, ed).Cambridge: Cambridge University Press;181–210.
Arak A, 1988. Callers and satellites in the natterjack toad: evolutionarily stable decision rules. Anim Behav 36:416-432.[CrossRef]
Arnqvist G, Rowe L, 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc R Soc Lond B 261:123-127.
Austad SN, 1984. A classification of alternative reproductive behaviours and a method for field-testing ESS models. Am Zool 24:309-319.
Ayre DJ, Coster P, Bailey WJ, Roberts JD, 1984. Calling tactics in Crinia georgiana (Anura: Myobatrachidae): alternation and variation in call duration. Aust J Zool 32:463-70.[CrossRef]
Bourne GR, 1992. Lekking behavior in the neotropical frog Ololygon rubra. Behav Ecol Sociobiol 31:173-180.
Bush S, 1993. Courtship and male parental care in the Majorcan mid-wife toad, Alytes muletensis (PhD dissertation). East Anglia: University of East Anglia.
Byrne PG, 2002a. Climatic correlates of breeding in the frog Crinia georgiana. J Herpetol 36:125-129.
Byrne PG, 2002b. The evolutionary significance of sperm competition in Australian anuran amphibians (PhD dissertation). Perth, Western Australia: The University of Western Australia.
Byrne PG, Roberts JD, 1999. Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana. Proc R Soc Lond B 264:95-98.
Byrne PG, Roberts JD, 2000. Does multiple paternity improve fitness of the frog Crinia georgiana ? Evolution 54:968-973.[CrossRef][Web of Science][Medline]
Byrne PG, Simmons LW, Roberts JD, 2002. Sperm competition selects for increased testes mass in Australian frogs. J Evol Biol 15:347-355.[CrossRef][Web of Science]
Byrne PG, Simmons LW, Roberts JD, 2003. Sperm competition and the evolution of gamete morphology in frogs. Proc R Soc Lond B 270:2079-2086.[Medline]
Cade W, 1979. The evolution of alternative male reproductive strategies in field crickets. In: Sexual selection and reproductive competition in insects (Blum MS, Blum NA, eds).New York: Academic Press; 343–379.
Church G, 1960a. Annual and lunar periodicity in the sexual cycle of the Javanese toad Bufo melanostictus. Schneider. Zoologica 44:181-88.
Church G, 1960b. The effects of seasonal and lunar changes on the breeding pattern of the edible Javanese frog, Rana cancrivora Gravenhorst. Treubia 25:214-33.
Clutton-Brock TH, Parker GA, 1995. Sexual coercion in animal societies. Anim Behav 49:1345-1365.[CrossRef]
Conner J, 1989. Density-dependent sexual selection in the fungus beetle, Bolitotherus cornatus. Evolution 43:1378-1386.[CrossRef][Web of Science]
Constanz GD, 1975. Behavioural ecology of mating in the male Gila topminnow, Poeciliopsis occidentalis (Cyprinodontiformes: Poeciliidae). Ecology 56:966-973.[CrossRef][Web of Science]
Davies NB, Halliday TR, 1979. Competative mate searching in male common toads,. Anim Behav 27:1253-1267.[CrossRef][Web of Science]
de Boer BA, 1981. Influence of population density on the territorial, courting and spawning behaviour of male Chromis cyanea (Pomacentridae). Behaviour 77:99-120.[CrossRef][Web of Science]
Donnelly MA, 1989. Effects of reproductive resource supplementation on space-use patterns in Dentrobates pumilio. Oecologia 81:212-218.[CrossRef][Web of Science]
D'Orgeix CA, Turner BJ, 1995. Multiple paternity in the red-eyed tree frog Agalychnis callidryas (Cope). Mol Ecol 4:505-508.[Medline]
Doty G, Welch AM, 2001. Advertisement call duration indicates good genes for offspring feeding rate in gray tree frogs (Hyla versicolor). Behav Ecol Sociobiol 49:150-156.[CrossRef][Web of Science]
Duellman, WE, Trueb, L, 1986. Biology of amphibians. New York: McGraw-Hill.
Emlen ST, 1976. Lek organization and mating strategies in the bullfrog. Behav Ecol Sociobiol 1:283-313.[CrossRef][Web of Science]
Emlen ST, Oring LW, 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
Fellers GM, 1979. Aggression, territoriality, and mating behaviour in North American treefrogs. Anim Behav 27:107-119.[CrossRef]
Fukuyama K, 1991. Spawning behaviour and male mating tactics of a foam-nesting treefrog, Rhacophorus schlegelli. Anim Behav 42:193-199.[CrossRef]
Gerhardt C, 1994. The evolution of vocalization in frogs and toads. Ann Rev Ecol Syst 2:293-324.[CrossRef]
Gerhardt HC, Roberts JD, Bee MA, Schwartz JJ, 2000. Call matching in the quacking frog (Crinia georgiana). Behav Ecol Sociobiol 48:243-251.[CrossRef][Web of Science]
Gross MR, 1982. Sneakers, satellites and parentals; polymorphic mating strategies in North-American sunfishes. Z Tierpsychol 60:1-26.[Web of Science]
Gross MR, 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92-98.[CrossRef][Web of Science]
Gwynne DT, 1984. Courtship feeding increases female reproductive success in bush-crickets. Nature 307:361-363.[CrossRef]
Halliday T, 1998. Sperm competition in Amphibians. In: Sperm competition and sexual selection (Birkhead TR, Møller AP, eds). London: Academic Press; 465–502.
Halliday TM, Tejedo M, 1995. Intrasexual selection and alternative mating behaviour. In: Amphibian biology, vol. 2 (Heatwole H, Sullivan BK, eds). Chipping Norton, NSW: Surrey Beatty and Sons; 469–517.
Höglund J, Robertson GM, 1988. Random mating by size in a population of common toads (Bufo bufo). Ethology 79:324-332.[Web of Science]
Howard RD, 1978a. The evolution of mating strategies in bullfrogs, Rana catesbiana. Evolution 32:850-871.[CrossRef][Web of Science]
Howard RD, 1978b. The influence of male-defended oviposition sites on early embryo mortality in bullfrogs, Rana sylvatica. Ecology 59:789-798.[CrossRef][Web of Science]
Howard RD, Kluge AG, 1985. Proximate mechanisms of sexual selection in wood frogs. Evolution 39:260-277.[CrossRef][Web of Science]
Jennions MD, Backwell PRY, Passmore NI, 1992. Breeding behaviour of the African frog Chiromantis xerampelina. Anim Behav 44:1091-1100.[CrossRef]
Jennions MD, Passmore NI, 1993. Sperm competition in frogs: testis size and a "sterile male" experiment on Chiromantis xerampelina (Rhacophoridae). Biol J Linn Soc 50:211-220.[CrossRef]
Jennions MD, Petrie M, 2000. Why do females mate multiply? a review of the genetic benefits. Biol Rev 75:21-64.[Medline]
Kluge AG, 1981. The life history, social organization, and parental behavior of Hyla rosenbergi Boulenger, a nest-building gladiator frog. Univ Mich Misc Publ No 169:1-170.
Kodric-Brown A, 1977. Reproductive success and the evolution of breeding territories in pupfish (Cyprinodon). Evolution 31:750-766.[CrossRef][Web of Science]
Kokko H, Johnstone RA, 2002. Why is mutual mate choice not the norm? operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signaling. Philos Trans R Soc Lond B 357:319-330.
Krupa JJ, 1989. Alternative mating tactics in the great plains toad. Anim Behav 37:1035-1043.[CrossRef]
Kusano T, Toda M, Fukuyama K, 1991. Testis size and breeding system in Japanese anurans with special reference to large testes size in the tree frog Rhacophorus arboreus. Behav Ecol Sociobiol 29:27-31.
Kvarnemo C, 1997. Food affects the potential reproductive rates of sand goby females but not of males. Behav Ecol 8:605-611.
Kvarnemo C, Ahnesjö I, 1996. The dynamics of operational sex ratios and competition for mates. Trends Ecol Evol 11:404-408.[CrossRef]
Kvarnemo C, Forsgren E, Magnhagen C, 1995. Effects of sex ratio on intra- and inter-sexual behaviour in sand gobies. Anim Behav 50:1455-1461.[CrossRef]
Kvarnemo C, Simmons LW, 1999. Variance in female quality, operational sex ratio and male mate choice in a bushcricket. Behav Ecol Sociobiol 45:245-252.[CrossRef][Web of Science]
Lucas JR, Howard RD, Palmer JG, 1996. Callers and satellites: chorus behaviour in anurans as a stochastic dynamic game. Anim Behav 51:501-518.[CrossRef]
Madsen T, Shine R, 1993. Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes. Am Nat 141:167-171.[CrossRef][Web of Science]
Main AR, 1965. Frogs of southern Western Australia. Perth: Western Australia Naturalist's Club.
McKinney F, Derrickson SR, Mineau P, 1983. Forced copulation in waterfowl. Behaviour 86:250-294.[CrossRef][Web of Science]
Mitchel SI, 1990. The mating system genetically affects offspring performance in woodhouse's toad (Bufo woodhousei). Evolution 44:502-519.[CrossRef][Web of Science]
Murphy CG, 1994. Chorus tenure of male barking frogs, Hyla gratiosa. Anim Behav 48:763-777.[CrossRef]
Otronen M, 1996. Effects of seasonal variation in operational sex ratio and population density on the mating success of different sized and aged males in the yellow dung fly Scathophaga stercoraria. Ethol Ecol Evol 8:399-411.
Perrill SA, Gerhardt HC, Daniel R, 1978. Sexual parasitism in the green treefrog Hyla cinerea. Science 200:1179-1180.
Perrill SA, Gerhardt HC, Daniel R, 1982. Mating strategies shifts in male green treefrogs (Hyla cinerea): an experimental study. Anim Behav 30:43-48.
Pröhl H, 2002. Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio. Behav Ecol 13:175-181.
Pyburn WF, 1970. Breeding biology of the leaf-frogs Phyllomedusa callidryas and Phyllomedusa dacnicolor in Mexico. Copeia 1970:209-218.[CrossRef]
Roberts JD, Standish RJ, Byrne PG, Doughty P, 1999. Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim Behav 57:721-726.[CrossRef][Web of Science][Medline]
Roberts WE, 1994. Explosive breeding aggregations and parachuting in a neotropical frog, Agalychnis saltator. J Herpetol 28:193-199.[CrossRef]
Rowe L, 1992. Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Anim Behav 44:189-202.[CrossRef][Web of Science]
Severinghaus LL, Kurtak BH, Eickwort GC, 1981. The reproductive behaviour of Anthidium maculatum (Hymenoptera: Megachilidae) and the significance of size for territorial males. Behav Ecol Sociobiol 9:51-58.[CrossRef][Web of Science]
Seymour RS, Roberts JD, 1995. Oxygen uptake by the aquatic eggs of the Australian frog Crinia georgiana. Phys Zool 68:206-222.
Shine R, 1979. Sexual selection and sexual dimorphism in the amphibia. Copeia 2:297–306.
Simmons LW, Tomkins JL, Hunt JC, 1999. Sperm competition games played by dimorphic male beetles. Proc R Soc Lond B 266:145-150.
Sinsch U, 1988. Temporal spacing of breeding activity in the natterjack toad, Bufo calamita. Oecologia 76:399-407.[Web of Science]
Smith MJ, Roberts JD, 2003a. Call structure may affect male mating success in the quacking frog Crinia georgiana (Anura: Myobatrachidae). Behav Ecol Sociobiol 53:221-226.[CrossRef][Web of Science]
Smith MJ, Roberts JD, 2003b. No sexual dimorphism in the frog Crinia georgiana (Anura: Myobatrachidae): an examination of pre and post-maturational growth. J Herpetol 37:132-137.[CrossRef]
Stewart MM, Pough FH, 1983. Population density of tropical forest frogs: relation to retreat sites. Science 221:570-572.
Stockley P, Searle JB, Macdonald DW, Jones CS, 1993. Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B 254:173-179.[Medline]
Sullivan BK, 1982. Male mating behaviour in the great plains toad (Bufo cognatus). Anim Behav 31:1011-1017.[CrossRef]
Sullivan BK, 1989. Mating system variation in Woodhouse's toad (Bufo woodhousii). Ethology 83:60-68.[Web of Science]
Sullivan BK, Ryan MJ, Verrel PA, 1995. Female choice and mating system structure. In: Amphibian biology vol 2 social behaviour (Heatwole H, Sullivan BK, eds). Chipping Norton, NSW: Surrey Beatty and Sons; 469–517.
Summers K, 1992a. Dart-poison frogs and the control of sexual selection. Ethology 91:89-107.[Web of Science]
Summers K, 1992b. Mating strategies in two species of dart-poison frogs: a comparative study. Anim Behav 43:907-919.[CrossRef]
Taborsky M, 1998. Sperm competition in fish ‘bougeois’ males and parasitic spawning. Trends Ecol Evol 16:222-227.
Thornhill R, 1979. Male and female sexual selection and the evolution of mating strategies in insects. In: Reproductive competition and sexual selection (Blum M, Blum N, eds).New York: Academic Press; 81–121.
Thornhill R, 1980. Rape in Panorpa scorpionflies and a general rape hypothesis. Anim Behav 28:52-59.[CrossRef]
Trivers RL, 1972. Paternal investment and sexual selection. In: Sexual selection and the descent of man (Campbell B, ed). Chicago: Aldine; 136–179.
Tuttle MD, Ryan MJ, 1982. The role of synchronized calling, ambient light and ambient noise in anti-bat predator behaviour of a treefrog. Behav Ecol Sociobiol 11:125-131.
Tuttle MD, Taft LK, Ryan MJ, 1982. Evasive behaviour of a frog in response to bat predation. Anim Behav 30:393-397.[CrossRef]
Wagner WEJ, Sullivan BK, 1992. Chorus organization in the Gulf Coast toad (Bufo valliceps): male and female behavior, and the opportunity for sexual selection. Copeia: 647–658.
Wells KD, 1977. The social behaviour of anuran amphibians. Anim Behav 25:666-693.[CrossRef]
Westneat DF, 1987. Extra-pair copulations in a pre-dominantly monogomous bird: observations of behaviour. Anim Behav 35:865-876.[CrossRef][Web of Science]
Widemo F, 1998. Alternative reproductive strategies in the ruff, Philomachus pugnax: a mixed ESS? Anim Behav 56:329-336.[CrossRef][Web of Science][Medline]
Woodward BD, 1986. Paternal effects on juvenile growth in Scaphiophus multiplacatus (the New Mexico spade-foot toad). Am Nat 128:58-65.
Woodward BD, 1987. Paternal effects on offspring traits in Scaphiopus couchi (Anura: Pelobatidae). Oecologia 73:626-629.[CrossRef][Web of Science]
Woolbright LL, Greene EJ, Rapp G, 1990. Density-dependent mate searching strategies of male woodfrogs. Anim Behav 40:135-142.
Yasui Y, 1998. The "genetic benefits" of multiple mating reconsidered. Trends Ecol Evol 13:246-250.[CrossRef]
Zimmerer EJ, Kallman KD, 1989. Genetic basis for alternative reproductive tactics in the pygmy swordtail. Xiphiphorus nigrensis. Evolution 43:1298-1307.[CrossRef][Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. A. Dziminski, J. D. Roberts, M. Beveridge, and L. W. Simmons Sperm competitiveness in frogs: slow and steady wins the race Proc R Soc B, November 22, 2009; 276(1675): 3955 - 3961. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. W Simmons, A. Denholm, C. Jackson, E. Levy, and E. Madon Male crickets adjust ejaculate quality with both risk and intensity of sperm competition Biol Lett, October 22, 2007; 3(5): 520 - 522. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Kokko and D. J Rankin Lonely hearts or sex in the city? Density-dependent effects in mating systems Phil Trans R Soc B, February 28, 2006; 361(1466): 319 - 334. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||