Calling is an honest indicator of paternal genetic quality in poison frogs

Several competing hypotheses have been put forward to explain why females of many species mate preferentially with males possessing the most conspicuous signals (e.g., ornaments, displays, or songs). We performed a laboratory experiment using two species of poison frogs, Dendrobates leucomelas and Epipedobates tricolor, to test the hypothesis that male calling performance is an honest indicator of parental quality. Our analyses are based on data from behavioral observations of mating activities of captive-reared individuals (and their offspring) that were housed in terraria for four consecutive breeding seasons. Male mating success increased with male calling rate and chirp duration in both species, suggesting that females preferred males with more elaborate calls. Because calling performance improved with age in D. leucomelas, female poison frogs that prefer males with more elaborate calls in the wild may end up mating with older males that have already proven their ability to survive. Females that mated with good callers obtained higher quality offspring. Eggs fertilized by males with high calling rates and long chirp durations had higher hatching success and produced tadpoles that were more likely to metamorphose into surviving frogs. As a consequence, females that mated with males with high calling performance obtained more surviving offspring per egg, compared to females that mated with poor callers. Collectively, our findings comply with the notion that female poison frogs prefer to mate with good callers because calling performance is a reliable predictor of offspring quality. The possible influence of maternal allocation and reasons for the strong effect size compared to previous studies are discussed.     

Chorusing Behaviour,a Density-dependent Alternative Mating Strategy in Male Common Toads (Bufo bufo)

Male chorusing behaviour was studied in a population of common toads (Bufo bufo) on the island of Öland south Sweden, and the functional role of male advertisement calling in this species was experimentally examined. Calling males were larger and heavier than non-calling males (t = 2.41, p < 0.025 and t = 2.36, p < 0.025, respectively). However, small males were also found to call. This indicates that large males persisted in calling for longer and/or called more often. The proportion of calling males decreased as population size increased during the breeding season, indicating that calling is a low density strategy. Females responded more readily to calls than males. There were insufficient data to determine if the dominant frequencies of advertisement calls were inversely correlated with male body size, however, this relationship was found for the similar release calls. Females were found not to discriminate between high and low frequency calls, but when given a choice between two calls of different sound pressure levels (SPL), females were attracted to the louder calls. Thus, the function of chorusing is to advertise the position of males to mate-seeking females when the population density is low.     

Stress hormone is implicated in satellite-caller associations and sexual selection in the Great Plains toad

The effects of androgens on male-typical traits suggest that variation among males in circulating levels can play a major role in sexual selection. We examined whether variation in vocal attractiveness is attributable to differences in androgen levels among Great Plains toads (Bufo cognatus). We found that noncalling "satellite" males practicing an alternative mating tactic were more likely to associate with males producing long calls. However, callers with satellites did not have higher androgen levels than callers without satellites. Rather, callers with satellites had significantly lower corticosterone (CORT) levels than callers without satellites. A CORT manipulation experiment suggested that differences in calls for males with and without satellites were related to differences in CORT levels. Furthermore, there was a negative correlation between CORT level and call duration within most nights of chorus activity. However, the correlation was weak for the pooled data (across all nights), suggesting that local environmental and/or social factors also affect call duration. Last, we show that females preferred broadcast calls of longer duration, characteristic of males with satellites and low CORT. These results imply that satellites optimize their reproductive success by associating with males producing long calls. However, this association should negatively affect the fitness of attractive callers.     

Plasticity of aggressive signalling and its evolution in male spring peepers, Pseudacris crucifer

Acoustic communication is important for determining and maintaining intermale spacing in breeding aggregations of anurans and insects. Because the number and proximity of signalling males can show extensive temporal and spatial variation, we should expect to find mechanisms that permit males to modify their signalling behaviour in ways that balance the needs to attract females and defend their calling space. We conducted two field playback experiments to investigate the role of plasticity in male aggressive signalling in intermale spacing of spring peepers (Anura, Hylidae). In the first experiment, we found a positive correlation between the amplitude of the advertisement calls of a male's nearest neighbour and the stimulus amplitude at which the male first produced aggressive calls. In the second experiment, repeated presentations of advertisement calls above a male's aggressive threshold resulted in rapid decreases in aggressive signalling and significant, but temporary, elevations of aggressive thresholds. We suggest that short-term habituation to a neighbour's calls could function as a proximate mechanism for plasticity in aggression that would allow males to accommodate nearby callers while also tracking fluctuations in the local density of calling individuals. In a third experiment, we examined female choice as an ultimate-level explanation for plasticity in male aggression. Females preferred advertisement calls to aggressive calls, but this preference was weak and was abolished by a 6-dB reduction in the amplitude of the advertisement call. We suggest that female preferences probably function as only one possible source of selection on plasticity in male aggressive signalling and propose energetic limitations as an additional source of selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Territoriality and Male Mating Success in the Dart-poison Frog,Epipedobates femoralis (Dendrobatidae,Anura)

The social and reproductive behaviour of the dart-poison frog, Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m² and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.     

Sexual differences in hormonal control of release calls in bullfrogs

Release calls in anuran amphibians are given when animals are inappropriately clasped by others. Since other call types, such as mate calls, are sexually dimorphic in frogs and toads, sonogram analysis was used to determine whether release call characteristics might also be sexually dimorphic in bullfrogs (Rana catesbeiana). Only intercall intervals differed significantly between males and females. Call duration, dominant frequency characteristics, and the display of secondary or tertiary harmonic frequencies were similar in both sexes. In the spring, but not the fall, calling rates were significantly lower in female bullfrogs, compared to males. Females also had significantly lower plasma androgen concentrations and higher plasma estrogen in the spring, compared to males. In both sexes, plasma androgen and estrogen were significantly higher in the spring, compared to the fall. The neuropeptide arginine vasotocin significantly decreased release call rates in females in the spring while it significantly increased rates in males. Vasotocin had no significant effect in the fall. Prostaglandin E2 significantly inhibited release calling in both males and females. On the other hand, prolactin significantly inhibited calling in female bullfrogs, but had no affect in males. Thus, although acoustic characteristics of release calls were similar in male and female bullfrogs, hormonal control of call rates was sexually dimorphic and seasonally variable.     

Mating strategy shifts in male green treefrogs (Hyla cinerea): An experimental study

Four field experiments were designed to study calling and satellite mating strategies in the green treefrog, Hyla cinerea. (1) The calling male was removed from 19 satellite associations and 11 of the 19 satellite males began calling. (2) After the calling male was removed from 10 satellite associations, a speaker broadcast synthetic mating calls. All of the satellite males oriented to the speaker. (3) Synthetic mating calls were played back to 14 calling males. Eleven males stopped calling and oriented to the speaker during at least one trial. (4) Sequences of synthetic mating calls and synthetic encounter calls were broadcast to 12 calling males. Nine males became satellites when the speaker emitted mating calls; none did so when encounter calls were presented.     

Acoustic mimicry and disruptive alternative calling tactics in an Australian bushcricket (Caedicia; Phaneropterinae; Tettigoniidae; Orthoptera): does mating influence male calling tactic?

Abstract.  Male calling and searching tactics are described for a duetting Australian bushcricket, Caedicia sp. 12 (Phaneropterinae; Tettigoniidae; Orthoptera). The repertoire of Caedicia sp. 12 consists of the calling song and, by nonduetting males, a series of calling tactics that include short-click calling, disruptive over-singing and a call mimicking the entire duet. Nonduetting males respond to the production of a duet by another male and a female with short-click calls that mimic the female call at the conclusion of a duet. By manipulating the male's mating history, it is found that this form of calling behaviour is more likely to occur within the male's 6-day postmating refractory period; the low cost tactic allows males to re-mate during spermatophore replenishment. Males also produce disruptive calls in response to a duet, where the male may over-sing the duetting male's signal or produce a call that appears to mimic the entire duet; the male produces a calling song followed by a short signal that has the same latency as the female's reply within a duet. Males also over-sing crucial elements of the duetting-male's song that are normally critical for the female's conspecific recognition. There is no evidence that females search for the duetting male partner, but males unable to enter a duet will search for the call of a responding female. Searching by males is more common when these males are producing disruptive calls. Alternative male calling tactics are discussed as a set of conditional strategies for securing unmated females.     

Female Preferences for Call Traits and Male Mating Success in the Neotropical Frog Physalaemus enesefae

Female preferences for male call traits may affect male mating success and the evolution of exaggerated secondary sexual traits. We used phonotaxis experiments to examine female preferences in the frog Physalaemus enesefae in relation to variation in male call duration, dominant frequency, intercall interval and amplitude (dB SPL). Females preferred long calls, low and average dominant frequency calls, short intercall intervals and more intense calls. We compared the patterns of female preferences with those of acoustic variation among males to test the prediction that properties with low within‐male variation are associated with stabilizing or weakly directional female preferences, whereas properties with high within‐male variation are associated with directional preferences. Females had weakly directional preferences for the dominant frequency of the call and strongly directional preferences for call duration and call rate. We also determined whether the temporal relationship between calls influenced preferences based on the dominant frequency of the call. Preferences for low‐frequency over high‐frequency calls disappeared when calls partially overlapped. Females preferred the leading call regardless of its dominant frequency. We also investigated mating patterns in the field. There was size‐assortative mating, as male and female body sizes snout‐vent length (SVL) were positively correlated. In addition, differences in the frequency distributions of body length (SVL) between mated and unmated males approached significance; lower SVL classes were underrepresented among mated males. These patterns may reflect female preferences for lower dominant frequency calls, as there is a negative correlation between male mass and the dominant frequency of the call.     

Factors affecting female sexual receptivity in the planthopper, Prokelisia dolus

Abstract. The mating system of Prokelisia dolus Wilson (Homoptera: Delphacidae) was characterized by determining: if males and females multiply mate; when transitions occur in female sexual receptivity, what triggers sexual refractoriness; and what behaviours characterize unreceptive virgins, receptive virgins, and unreceptive mated females. Males copulated with up to six females in less than 1 h, but completely inseminate, on average, only the first four females. Females rarely mated more than once, unless males were depleted of sperm due to previous copulations or if copulation was interrupted (if duration was<2 min). Male and female calling was associated (100% and 91%, respectively) with sexual receptivity and resultant matings. The transition from unreceptive virgin to receptive (calling) mature virgin occurred 48 h posteclosion, and all were mated by day 4. Females that were sexually immature and those completely inseminated did not call. Rejection of males by females included walking away from approaching males (65%), female kicking (7%), and abdominal lifting (5%). Rejection of males was observed by immature, mature and calling, and mated females. Sexual refractoriness was not triggered by acoustic and visual stimuli or mechanical stimulation of genitalia. Refractoriness was also not triggered by reception of small quantities of sperm because some females laid a few viable eggs yet calling was not terminated. Sexual refractoriness was activated by a substance in the ejaculate as demonstrated by injection into the haemocoel of male accessory glands or testes and homogenates of seminal vesicles. This is the first study that documents the role of male ejaculate in inhibiting female sexual receptivity in Hemiptera (Homoptera).     

Calling Behaviour Influences Mating Success in Male Painted Reed Frogs,Hyperolius marmoratus

A detailed study was made of the natural calling behaviour of male painted reed frogs in the wild. Comprehensive minute by minute records of the vocal activity of males calling simultaneously in the breeding chorus were generated over a 19-night period using a multi-channel event recorder. With few exceptions, the period over which males called either spanned or extended beyond the time window when females sought mates in the chorus. Males varied little in calling persistence and the majority produced advertisement calls during each minute of the calling period. Aggressive interactions between males curtailed advertisement call production but fights were short-lived, seldom repeated and limited to a small proportion (12.6%) of males. Call rate was independent of body size and varied widely among males active in the chorus at the same time and under the same environmental conditions. The relative call rate ranks of individuals were sustained over time. The call rates of mated males were high in relation to the rates of other males monitored in the chorus at, and prior to, the time of mating. Females usually preferred the higher of two call rate alternatives presented in a range of two-choice phonotaxis experiments.     

The function of Barbary macaque copulation calls.

In a wide variety of animal species, females produce vocalizations specific to mating contexts. It has been proposed that these copulation calls function to incite males to compete for access to the calling female. Two separate advantages of inciting male-male competition in this way have been put forward. The first suggests that as a result of calling, females are only mated by the highest ranking male in the vicinity (indirect mate choice hypothesis). The second proposes that copulation calling results in a female being mated by many males, thus promoting competition at the level of sperm (sperm competition hypothesis). In this paper, I give results from the first experimental study to test these hypotheses. Playback was used to examine the function of copulation calls of female Barbary macaques (Macaca sylvanus) in Gibraltar. Although rank did not affect lone males'' likelihood of approaching copulation calls, when playbacks were given to pairs of males only the higher ranking individual approached. Moreover, females were mated significantly sooner after playback of their copulation call than after playback of a control stimulus. These results suggest that the copulation calls of female Barbary macaques play a key role in affecting patterns of male reproductive behaviour, not only providing an indirect mechanism of female choice, but also promoting sperm competition by reducing the interval between copulations. Potential fitness benefits of inciting male-male competition at these two levels are discussed.     

Intrasexual selection and group spawning in quacking frogs (Crinia georgiana)

In the Australian frog Crinia georgiana, matings frequentlyinvolve a single female and multiple males (group spawning).The aim of the present study was to demonstrate a connectionbetween 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 breedingperiod, male density and OSR varied substantially and were significantlyinfluenced by climatic conditions. The frequency of agonisticinteractions between males was higher in denser choruses. Fightswere typically over the possession of sites used to broadcastadvertisement calls and were almost always won by larger males.At higher densities, males allocated significantly less timeto calling to attract females and spent more time as nonmovingsatellites or roaming through an aggregation (searching). However,large males always called more than did small males. The numberof males involved in a spawning correlated positively with variationin both male density and OSR. Observation of group spawningsrevealed that they generally arose when a satellite male joineda mating pair after a female chose to mate with a calling maleor when a female was seized by a searching male and the pairwas joined by other searching males. These findings, coupledwith past research documenting costs but no benefits of multiplepaternity to females, suggest that competitively inferior malesforce group spawns.     

Acoustic satellite behaviour in the Australian bushcricket Elephantodeta nobilis (Phaneropterinae, Tettigoniidae, Orthoptera)

Male and female Elephantodeta nobilis duet with the female responding to the male's long and complex call. The duetting male's call consisted of four parts, described here as parts A, B, C and D. We found that the female replied 570 ms after the male's D pulse, which followed the extended part B and short click of part C. Noncalling males were attracted to the duet and often used satellite tactics by inserting a volley of clicks 200 ms before the alpha male's D pulse. Satellite males used part C of the alpha male song to cue their own call and this inserted call induced females to reply earlier compared with the alpha male call alone. Alpha males often extended their calls with additional D-type calls and so we examined the effectiveness of these calls as countermeasures to satellite calling. There was no influence of this alpha strategy on the satellite's propensity to call although more calls from the alpha male did cause the female to reply more frequently. We also examined the effect of relative intensity of alpha and satellite calls on the female's reply. Reduced satellite intensity increased the variance in the timing of the female response. Finally, we tested the effectiveness of the satellite's call on female phonotaxis within a two-speaker arena. Although females preferred the alpha male they were nevertheless attracted to the satellite calls regardless of the latter's relative intensity. We discuss the possible role of satellite calling as a novel conditional strategy. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mating tactics and male wing dimorphism in the damselfly,Mnais pruinosa costalis selys (Odonata: Calopterygidae)

Males of the damselfly,Mnais pruinosa costalis, exhibit wing color dimorphism: one form has orange wings, and the other hyaline wings which resemble female wings. The former is usually territorial and the latter uses sneaky mate securing tactics. When orange-winged males failed to establish territory, they became floaters that day. Hyaline-winged males perched around their territories and often, formed in tandem without any apparent courtship behavior when they found females. Their copulation frequency was higher and copulation duration longer than those of territorial males. A few females oviposited without remating. Total oviposition duration of females with which a hyaline-winged male mated was more than 32 min per male on average in a day Females that copulated with hyaline-winged males often remated with orange-winged residents before oviposition. Total duration of oviposition bouts of females after mating with floaters was short (15 min), while that with territorial residents was long (66 min). As a result, total oviposition duration of females with which an orange-winged male mated was about 40 min in a day. The reproductive success of the hyaline-winged males may be similar to that of the orange-winged males.     

Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans

Males of most anuran species (frogs and toads) vocalize to attractmates. However, individuals of many vocal species may also adoptalternative noncalling "satellite" tactics. Satellite malescharacteristically remain in close proximity to calling conspecificsand attempt to intercept incoming females attracted to advertisingmales. Emerson proposed that alternation between calling andnoncalling behavior in anurans is mediated by a reciprocal interactionbetween circulating levels of corticosterone and androgens thatis driven by depletion of energy reserves during vocalization.We tested this hypothesis by examining steroid hormone profilesand the relative body condition of calling and satellite Woodhouse'stoads (Bufo woodhousii) and Great Plains toads (B. cognatus).Consistent with Emerson's hypothesis, callers had significantlyhigher circulating corticosterone levels and were in bettercondition than satellites. However, levels of testosterone anddihydrotestosterone did not differ significantly between satellitesand callers, and we found no evidence that high levels of corticosteronehad an inhibitory effect on androgen production in either species.These data thus support a relationship between corticosteronelevels and depletion of energy reserves during bouts of vocalizationbut suggest that alternation between calling and satellite behaviormay be associated with direct effects of corticosterone on brainvocal control centers. We propose a model that incorporatesrelationships among energy reserves, androgens, corticosterone,and arginine vasotocin-producing neurons in the telencephalonto explain transitions between calling and satellite tacticsin toads.     

The effect of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus

1. In many organisms, males provide nutrients to females via ejaculates that can influence female fecundity, longevity and mating behaviour. The effect of male mating history on male ejaculate size, female fecundity, female longevity and female remating behaviour in the seed beetle Callosobruchus maculatus was determined.
2. The quantity of ejaculate passed to females declined dramatically with successive matings. Despite the decline, a male's ability to fertilize a female fully did not appear to decline substantially until his fourth mating.
3. When females multiply mated with males of a particular mated status, the pattern of egg production was cyclic, with egg production increasing after mating. Females multiply mated to virgins had higher fecundity than females mated to non-virgins, and females mated to twice-mated males had disproportionately increased egg production late in their life.
4. Females that mated to multiple virgins, and consequently laid more eggs, experienced greater mortality than females mated only once or mated to non-virgins, suggesting that egg production is costly, and rather than ameliorating these costs, male ejaculates may increase them by allowing or stimulating females to lay more eggs.
5. Females mating with non-virgin males remated more readily than did females mated to virgins. Females given food supplements were less likely to remate than females that were nutritionally stressed, suggesting that females remate in part to obtain additional nutrients.     

The Relationship Between the Presence of Satellite Males and Nest-Holders' Mating Success in the Azorean Rock-Pool Blenny Parablennius sanguinolentus parvicornis

In the Azorean rock-pool blenny, sexually active males may adopt alternative reproductive tactics. In the present paper the relationship between the presence of satellite males and the reproductive success of nest-holders was investigated by comparing nests with and without an associated satellite male. Males with an associated satellite male suffered more conspecific intrusions but they did not display a higher frequency of attacks towards conspecifics. Nest-holder males were more aggressive towards other conspecifics than towards satellites and the tolerance of nest-holders towards satellites was inversely correlated with the time spent by the satellites in the breeding territory, which suggests control by the nest-holder male of the satellite investment in shared territorial defence. Nest-holders with an associated satellite male had higher condition factors and received more female visits and more spawnings. These results bear two possible interpretations. (1) Nest-holders benefit from the presence of a satellite male by increased attractiveness of their nests to females; satellite males are mutualists helping to defend the nest-owner's territory and to attract females, which is why they are tolerated. (2) Satellite males associate preferentially with more successful nest-holder males which have higher condition factors, and by doing so have more opportunities to achieve parasitic fertilizations. Only experiments will allow these two hypotheses to be distinguished.     

Social Correlates of Variation in Male Calling Behavior in Blanchard's Cricket Frog,Acris crepitans blanchardi

I studied variation in male calling behavior and its social correlates in Blanchard's cricket frog, Acris crepitans blanchardi. Calls were produced in distinct call groups, and they increased in duration and complexity from the beginning to end of a call group. Dominant frequency was the only character of 18 quantified consistently correlated with male snout-vent length. Calls from the beginning of a call group varied independently of calls from the middle and end of a call group, and only calls from the beginning of a call group exhibited significant variation among males, thus relative consistency within males. Other characters varied greatly within individual males. Unlike most other anurans, dominant frequency also exhibited tremendous within-male variation. The relative influence of caller density, local caller density, nearest neighbor distance, and nearest neighbor sound pressure level on variation in male calling behavior was examined. Nearest neighbor distance, mediated through the sound-pressure level of neighbor calls, appeared to have the greatest influence on variation in male calling behavior. The most profound changes in calling behavior occurred during aggressive encounters; males altered their calling behavior in a manner suggesting that they respond to competitors with graded aggressive signals. Furthermore, the structure of the communication system suggests that calls are graded not only in response to the level of social competition, but graded over a call group as well.     

The mating behaviour of the egyptian cotton leafworm moth, spodoptera littoralis (Boisd.)

A detailed study of courtship in Spodoptera littoralis showed that there were four significant behaviour patterns. The male flew to a calling female and hovered above her with his brushes fully extended. In response, the female lifted her wings, curved her abdomen and withdrew her pheromone gland. The male settled beside the female to pair and then moved to hang head downwards during copulation. Thirty percent of successful courtships lacked one of the main behaviour patterns. Nearly half the courtships observed did not end in copulation: none of these included all of four major behaviour patterns and the majority lacked two or three. Females often rejected males with a rapid flick of the wings. Antennaless males did not mate or extend the brushes in response to a calling female. Just over half of the antennaless females observed during 135-min tests mated with normal males, but courtship was abnormal. Olfactory cues appeared to be important to females in recognizing the courting male, since antennaless females did not wing flick, were significantly more likely to take to flight as the result of the male brush display and frequently failed to retract the pheromone gland during the latter states of courtship. The courtship behaviour of S. littoralis is compared with published accounts for other Noctuids.