Male Calling Behavior and Female Choice in the Neotropical Treefrog Hyla microcephala

The effect of stimulus call complexity and calling rate on the vocal responses of males and female mate choice was studied in Hyla microcephala in Panama. Males increased the number of notes in their calls in response to increases in stimulus call complexity during both playback of 1 to 8-note advertisement calls and during natural interactions. However, precise matching of the number of notes in stimuli and responses did not occur consistently. Males also increased calling rates if stimuli were presented above prestimulus rates. Two-stimulus choice experiments demonstrated that females prefer both higher calling rates and greater call complexity, indicating that the ways males change their vocal behavior during interactions increases their attractiveness to potential mates. Tests in which the relative intensity of a high and low rate stimulus was varied indicated that females prefer stimuli with higher total sound energy. In a natural chorus, it is likely that females simply approach males giving the most conspicuous calls.     

Acoustic Preference of Frog‐Biting Midges (Corethrella spp) Attacking Túngara Frogs in their Natural Habitat

In many animals, males aggregate to produce mating signals that attract conspecific females. These leks, however, also attract eavesdropping predators and parasites lured by the mating signal. This study investigates the acoustic preferences of eavesdroppers attracted to natural choruses in a Neotropical frog, the túngara frog (Engystomops pustulosus). In particular, we examined the responses of frog‐biting midges to natural variation in call properties and signaling rates of males in the chorus. These midges use the mating calls of the frogs to localize them and obtain a blood meal. Although it is known that the midges prefer complex over simple túngara frog calls, it is unclear how these eavesdroppers respond to natural call variation when confronted with multiple males in a chorus. We investigated the acoustic preference of the midges using calling frogs in their natural environment and thus accounted for natural variation in their call properties. We performed field recordings using a sound imaging system to quantify the temporal call properties of males in small choruses. During these recordings, we also collected frog‐biting midges attacking calling males. Our results revealed that, in a given chorus, male frogs calling at higher rates and with higher call complexity attracted a larger number of frog‐biting midges. Call rate was particularly important at increasing the number of midges attracted when males produced calls of lower complexity. Similarly, call complexity increased attractiveness to the midges especially when males produced calls at a low repetition rate. Given that female túngara frogs prefer calls produced at higher repetition rates and higher complexity, this study highlights the challenge faced by signalers when increasing attractiveness of the signal to their intended receivers.     

Mate selection in Litoria chloris and Litoria xanthomera: Females prefer smaller males

It is generally accepted that high quality males are those that succeed in male–male competition: in either aggression or rivalry to attract and be selected by females. Previous studies of amphibians have suggested that the main characters influencing male mating success include variation in call characteristics (e.g. call rate, call intensity), calling behaviour, body condition, age and chorus tenure. In the present paper, several of the characters influencing female mate choice (male body size, body condition, call rate, call frequency and chorus tenure) are investigated in two closely related, explosive breeding frog species Litoria chloris and Litoria xanthomera. Smaller males of both species are shown to be more successful than larger males and this success is attributed to the increased chorus tenure of smaller males in L. xanthomera. This increased chorus tenure was attributed to the lower total energy used per call by a small male calling at a higher frequency. Whether increased chorus tenure explains female mate choice in L. chloris is uncertain but is highly probable given the strong similarity between the two species in both ecology and call characteristics.     

Social Context Influences Androgenic Effects on Calling in the Green Treefrog (Hyla cinerea)

Courtship behavior in frogs is an ideal model for investigating the relationships among social experience, gonadal steroids, and behavior. Reception of mating calls causes an increase in androgen levels in listening males, and calling, in turn, depends on the presence of androgens. However, previous studies found that androgen replacement does not always restore calling to intact levels, and the relationship between androgens and calling may be context dependent. We examined the influence of androgens on calling behavior in the presence and the absence of social signals in male green treefrogs (Hyla cinerea). We categorized calling during an acoustic stimulus (mating chorus or tones) as evoked and calling in the absence of a stimulus as spontaneous. Intact males received a cholesterol implant, castrated males were castrated and received a cholesterol implant, and T-implanted males were castrated and received a testosterone implant. The androgen levels (mean +/- SE ng/ml of plasma) achieved by the implants were as follows: castrated males, 1.2 +/- 0.2; intact males 21.9 +/- 7.0; T-implanted males, 254.6 +/- 39.5. As in other frogs, calling depends on the presence of androgens, as castration abolished and T replacement maintained calling. However, among intact and T-implanted males, the influence of androgens on calling differed between spontaneous and evoked calling. There was a positive effect of androgen treatment on spontaneous call rate and a positive correlation between spontaneous call rate and androgen levels. The influence of androgen levels on evoked call rate was more complex and interacted with acoustic treatment. Surprisingly, T implants suppressed the chorus-specific increase in calling that is evident in intact males. In addition, in response to the chorus, T-implanted males called less than did intact males, in spite of higher androgen levels. Furthermore, variation in androgens did not explain variation in evoked call rate. These data indicate that androgens influence the motivation to call, but that, when socially stimulated, androgens are necessary but insufficient for calling.     

Individual, nightly, and seasonal variation in calling behavior of the gray tree frog, Hyla versicolor: implications for energy expenditure

We investigated individual, nightly, and seasonal variationin calling behavior of a population of gray tree frogs (Hylaversicolor) from Connecticut, USA. Repeated recordings of individualmales on seven nights revealed significant differences amongmales in calling rate on all but one night and differences innumber of pulses per call and number of pulses produced perhour (pulse effort) on four nights. Most males reduced callingactivity late at night (after 2230 h), but some maintained arelatively steady rate of call production before dropping outof the chorus. Data collected for 26 individuals recorded onthree or more nights throughout the breeding season revealedsignificant differences among males in calling rate, numberof pulses per call, and pulse effort, but repeatabilities forall three variables were low (0.17, 0.35, and 0.12, respectively).The highest repeatability was for number of pulses per call,a variable strongly influenced by proximity to calling neighbors,probably because males often interacted with neighbors at similardistances on several successive nights. Males tended to reducethe number of pulses per call as the season progressed and thedistance between neighbors decreased, but they showed no clearseasonal change in calling rate or pulse effort. There was asubstantial seasonal decline in the number of hours of chorusactivity, resulting in a median decrease of 43% in nightly energyexpenditure by calling males.     

The Sounds of Silence as an Alarm Cue in Túngara Frogs,Physalaemus pustulosus

In many species males vocally advertise for mates in choruses and these choruses serve as acoustic beacons to conspecific females as well as to eavesdropping predators and parasites. Chorusing will often cease in response to disturbances, such as the presence of predators. In some cases the cessation is so rapid and over such a large area that it seems improbable that males are all responding directly to the same local disturbance. Here, we demonstrate experimentally in Neotropical túngara frogs, Physalaemus pustulosus, that the cessation of calling by males spreads rapidly through the chorus. The cessation of chorusing in response to the cessation of playbacks of three calling males is more effective in inducing chorus cessation than is the cessation of one male calling. When three males are calling, the cessation of complex calls is more effective in inducing chorus cessation than simple calls. There is no main effect on whether the final call of the male is complete or is interrupted. We thus conclude that the sudden lack of signals—the ‘sounds of silence’—becomes an alarm cue that can explain the rapid cessation of choruses that are common in many chorusing species.     

Calling behavior and directional hybridization between two toads (Bufo microscaphus x B. woodhousii) in Arizona

Male calling effort and mitochondrial DNA (mtDNA) variation were examined in a breeding chorus of toads from a hybrid zone between Bufo microscaphus and B. woodhousii in central Arizona. The chorus comprised 50 B. microscaphus and 17 hybrids, identified on the basis of morphology and advertisement calls; no pure B. woodhousii were observed. Males produced advertisement calls throughout the early evening, even when relatively large numbers of males (>50) were present at the chorus; active searching and satellite tactics were not observed. Calling efforts (call duration x call rate) of hybrids (23.9%, n = 8) and B. microscaphus (24.9%, n = 19) were similar and comparable to call efforts of B. woodhousii (21.9%, n = 10) from a different site. Moreover, repeatabilities of calling effort were significant (r = 0.45) for hybrid males, but not for B. microscaphus and B. woodhousii. Thus, calling behavior of hybrid males was neither significantly reduced nor more variable than that of their parental species. The distribution of mtDNA haplotypes revealed directional introgression is occurring between male B. microscaphus and female B. woodhousii: All 17 hybrids possessed B. woodhousii mtDNA. The proximate mechanism driving hybridization appears to involve common male (B. microscaphus) and rare female (B. woodhousii) matings as B. woodhousii expands its range.     

Inter-male Spacing and Aggression in African Painted Reed Frogs,Hyperolius marmoratus

Inter-male spacing and the role of aggression in the maintenance of spatial organization was examined in choruses of Hyperolius marmoratus males housed in a semi-natural enclosure. The effects of chorus size on spacing patterns, nearest neighbour distances and male aggressive behaviour were examined. Males were found to reduce nearest neighbour distances as chorus size increased. This was accompanied by a shift in spacing pattern from even in small choruses (5–9 males) to random in choruses of 10 to 13 males. In choruses of 14, spacing patterns were once again even. The reason for these shifts is unclear but may reflect a sudden, rather than gradual increased tolerance by individuals to high neighbour call intensity as space to call from becomes more limited. The level of male aggression was influenced by chorus size and the time of night. In general, more aggressive interactions occurred in high density choruses. However, this did not translate into higher levels of individual male aggression as density increased. Individual male aggression was high in early evening choruses and declined to a minimum at peak chorusing time. High levels of aggression during early evening may reflect the establishment of calling sites by males, while the drop in aggression at peak chorusing time may occur in response to the presence of females in the chorus at this time or as a consequence of masking of neighbours calls.     

Energetics of calling and metabolic substrate use during prolonged exercise in the European treefrog Hyla arborea

Rates of oxygen consumption and carbon dioxide release were measured in calling and resting European tree frogs using open-flow-through respirometry. The energetic cost of calling was high with an average of 1.076 ml O₂/(g · h) at average call rates of 8000 calls/h. The maximum factorial metabolic scopes averaged 24 with momentary peak values ranging between 5 and 41. There was a threefold difference in O₂-consumption between individual males calling at the same rate. Respiratory quotients indicated that both lipids and carbohydrates were used to fuel calling. Carbohydrates provided the major fuel (69% on average) with dependence on carbohydrates increasing with call rate. In contrast to marathon runners, there was no shift in metabolic substrate use over a calling period of 2–3 h. Accepted: 25 September 2000     

Patterns of fish calling in a nearshore environment in the Great Barrier Reef

Long-term sea-noise statistics have been obtained from a region of the central section of the Great Barrier Reef. Fish calling was a major contributor to sea-noise levels. Calling was either in choruses, where groups of fishes called en masse, or as isolated calls repeated ad nauseam. Four calling types predominated, with each displaying unique call characteristics and calling patterns through time and space. Analysis of call types offered information on the fish's calling physiology, behaviour and, through the call's interaction with the local environment, on the location of the caller. Call types ranged from less than 10 ms to several seconds long, and were comprised from one to nearly 40 pulses. The structure of each pulse was related to swim-bladder mechanics; normally swim-bladders were lightly damped. Fish calling was most common during the Australian summer with one call type also displaying lunar trends. All calls had daily patterns of sound production with highest activity levels generally at night. There was some spatial separation of zones of highest call rates, but sources avoided competition for the 'sound space' primarily by offsetting the time of chorus or maximum call rate. On some occasions, a call type attributed to nocturnal planktivorous fishes may have ensonified much of the Great Barrier Reef.     

The neuropeptide arginine vasotocin alters male call characteristics involved in social interactions in the grey treefrog, Hyla versicolor

We investigated the effects of different doses (0, 2.5, 25 and 250 μg) of the neuropeptide arginine vasotocin (AVT) on the calling characteristics of the grey treefrog in a chorus in its natural habitat. AVT changed some call characteristics known to influence social behaviour in grey treefrogs. It increased call duration and number of pulses in a call, but not dominant frequency, call rate or pulse effort. Saline injections and handling did not produce significant changes in any of the call characteristics. In addition, individual animals injected with AVT only rarely produced call characteristics that were outside of the range found in the preinjection measurements, suggesting that AVT does not cause abnormal calling behaviour. Other researchers have demonstrated that longer calls with more pulses are produced by males when chorus densities increase, and females display a strong preference for longer calls with more pulses. This suggests that the changes induced by AVT injections may have functional consequences in social interactions. We previously demonstrated that AVT-injected males (25 μg AVT) displaced resident males from calling sites through changes in calling behaviour under natural field conditions. Our results indicate that changes in call duration and pulse number could contribute to the unmanipulated resident male's behaviour towards the AVT-injected intruder, perhaps because the calls are more attractive to females or because the calls are perceived as more aggressive. Copyright 2000 The Association for the Study of Animal Behaviour.     

Dynamic properties of the advertisement calls of gray tree frogs: patterns of variability and female choice

We assessed the potential for several acoustic properties ofthe advertisement calls of male gray tree frogs to affect relativemating success by relating patterns of variation in these propertiesto minimum differences required to elicit female choice. Dynamicproperties (pulse number, PN; call rate, CR; and duty cycle,DC, the ratio of call duration to call period) varied much morewithin bouts of calling than a static property (dominant frequency,DF) but nevertheless exhibited significant between male variationin three of four breeding seasons. Many multiply recorded malesconsistently produced calls with values substantially aboveor below mean values of males recorded on the same nights. Nightlyranges of variation in PN and CR were often greater than theminimum differences required to elicit female preferences inthe laboratory. In most experiments, females chose high-PN orfast-CR calls over low-PN or slow-CR alternatives, respectively,even if the preferred stimuli were farther away or 6-10 dB lowerin sound pressure level (SPL), provided that differences inPN or CR were 100%. Consistent with these results, females didnot always choose the closer of two calling males in the field.Nightly ranges of variation in DF rarely equaled the minimumdifference required to elicit SPL independent preferences. Femalespreferred a stimulus of high-PN and slow-CR over an alternativeof low-PN or fast-CR with the same acoustic on-time; in twoexperiments, females chose calls of high-PN over low-PN alternativeseven though the playback of the high-PN call was interruptedand the low-PN call was broadcast continuously. Thus, femalepreferences were not merely based on the total time of acousticstimulation. Responses of females tested twice in the same experimentsuggest that phenotypic variation in preference was limitedin our study populations.     

Chorusing Behaviour in the Lusitanian Toadfish: Should I Match My Neighbours' Calling Rate?

Choruses have been described mostly in birds, anurans and insects but have been poorly studied in fish. Research in batrachoidid (toadfishes) species suggest vocal facilitation among neighbouring males, but whether chorusing fish present more complex interactions is unknown. In this study, we test the hypothesis that chorusing fish males compete actively to increase attractiveness to females. We first describe vocal interactions in natural choruses of Lusitanian toadfish males. Our analysis found positive correlations between the calling rates of neighbouring males in several occasions. However, we also found that males that showed an overall low vocal activity throughout the observation period exhibited peaks of increased calling activity when neighbours decreased their calling rate, suggesting an opportunistic maximisation of attractiveness. We further test with playback experiments how toadfish males adjust calling activity relative to their neighbours'. We observed that males silent at the time of the playbacks but who had an overall high vocal performance tended to start calling when exposed to playbacks in contrast to low‐activity males. Playback experiments further showed that males initially calling at a high rate adjust their calling rate according to the neighbour's vocal activity level, that is, they increased calling rate when exposed to a high calling rate and decreased it when confronted with a low calling rate. However, males calling at a low rate did not significantly alter their calling rate when presented with a low (similar) or higher calling rate, probably due to temporary physiological and/or ecological constraints. We argue that Lusitanian toadfish males tend to optimise calling effort in relation to their neighbours when they are actively advertising. Further studies are necessary to better understand vocal behaviour with increased chorus size.     

Diel Calling Activity and Field Survival of the Bushcricket,Sciarasaga quadrata (Orthoptera: Tettigoniidae): A Role for Sound-locating Parasitic Flies?

In this study I examine the variability in calling activity of Sciarasaga quadrata over both the short (4 d) and long term (life span), and the temporal pattern to host searching by its most significant natural enemy, the ormiine fly Homotrixa alleni. Indeed, few male S. quadrata survive the entire calling season as this acoustically orienting parasitoid fly continually ‘culls’ calling males out of the population. I found that male S. quadrata commence calling over 1 h before sunset, cease around midnight and call, on average, for over 3 h within this period (range 0–11 h 09 min). There was significant concordance and repeatability in calling activity over both the short and long term, enabling me to conclude that relative differences in calling activity among males persist throughout a male's life span. There was a distinct peak to host searching by gravid female flies, with 82 % of all flies collected at acoustic traps between sunset and midnight. A positive association between call duration (time spent calling) and fly attraction was evident from multiple collections of flies at single traps. Counter to expectation, there was no significant decline in average call duration across successive collections of males, indicating that long-call-duration males were not being selectively culled by flies from the calling population. Males at the end of the calling season, when their remaining reproductive potential is low, allocate the majority of their calling time between sunset and midnight despite the high risk of fly attack. The distribution of call durations within the population was not skewed, which if heritable, indicates a lack of history of directional selection acting on call duration. Limited evidence suggests that encounters with females are rare in S. quadrata so that males may be selected, irrespective of natural selection pressure, to call for long periods of time to optimize their chance of attracting mates. The above findings are further discussed in relation to parasitoid foraging and acoustic reproductive strategies.     

Acoustic Competition in Male Midwife Toads Alytes obstetricans and Alytes cisternasii: Response to Neighbor Size and Calling Rate. Implications for Female Choice

Effects of neighbor on male calling behavior was studied through playback experiments of synthetic calls to males of two species of midwife toads. The responses of resident males were scored considering two temporal parameters (call duration and calling rate) and one spectral parameter (dominant frequency). The sounds used for the playback tests included two levels of fundamental frequency (correlated with male size) and two levels of call repetition rate. In both species, resident males only changed their calling rate in the presence of an intruder, and the response was different for synthetic calls with two levels of dominant frequencies and with two calling rates. Resident size was not significantly correlated with the magnitude of the change in the calling rate. On the other hand, resident calling rate was significantly and positively correlated with the magnitude of the increase in calling rate of the stimulus. The maximum relative increase in calling rate was observed in A. cisternasii. In phonotaxis tests, females are preferentially attracted to calls emitted at a higher rate confirming the importance of changes in calling rate for female attraction.     

A rain forest dusk chorus: cacophony or sounds of silence?

A rain forest dusk chorus consists of a large number of individuals of acoustically communicating species signaling at the same time. How different species achieve effective intra-specific communication in this complex and noisy acoustic environment is not well understood. In this study we examined acoustic masking interference in an assemblage of rain forest crickets and katydids. We used signal structures and spacing of signalers to estimate temporal, spectral and active space overlap between species. We then examined these overlaps for evidence of strategies of masking avoidance in the assemblage: we asked whether species whose signals have high temporal or spectral overlap avoid calling together. Whereas we found evidence that species with high temporal overlap may avoid calling together, there was no relation between spectral overlap and calling activity. There was also no correlation between the spectral and temporal overlaps of the signals of different species. In addition, we found little evidence that species calling in the understorey actively use spacing to minimize acoustic overlap. Increasing call intensity and tuning receivers however emerged as powerful strategies to minimize acoustic overlap. Effective acoustic overlaps were on average close to zero for most individuals in natural, multispecies choruses, even in the absence of behavioral avoidance mechanisms such as inhibition of calling or active spacing. Thus, call temporal structure, intensity and frequency together provide sufficient parameter space for several species to call together yet communicate effectively with little interference in the apparent cacophony of a rain forest dusk chorus.     

Female begging in European robins: do neighbors eavesdrop for extrapair copulations?

Female European robins beg for food from their mates throughoutthe breeding season using far-carrying "seep" calls which resemblethe begging calls of fledglings. We investigated the possibilitythat these calls are eavesdropped by neighboring males andused as cues to target intrusions during the fertile period.Female seep calling and male courtship feeding peaked in thefertile period, and males appeared to modify provisioning rate in relation to seep calling rate. Further, there was a positivecorrelation between rate of courtship feeding and clutch size,both of which tended to be inversely related to seep callingrates. These observations imply that the seep call is a hungersignal directed at pair males. As the signal is loud and givenmost frequently during the fertile period, it must also contain information about fertility and location. Playback experimentssuggested that this information is eavesdropped by neighboringmales, who responded to rapid rates of seep calling more readilythan slow rates and to calls broadcast at the edge of territoriesrather than their center, presumably in search of extrapaircopulations. Pair males can reduce the intensity of the female's signal by courtship feeding, and thus male provisioning mayprotect paternity.     

Individual variation in morphological, physiological, and biochemical features associated with calling in spring peepers (Pseudacris crucifer)

In an eastern North American tree frog, the spring peeper (Pseudacris crucifer), calling rate has been correlated with reproductive success in the field. To determine the sources of individual variation in calling rate in this species, I analyzed males calling at rates greater than and less than the chorus average throughout one breeding season. Compared to low-rate callers, high-rate callers were relatively larger, heavier, older, and in better body condition, and their muscles used in calling had higher activities of the enzymes citrate synthase and beta-hydroxyacyl-CoA dehydrogenase. This muscle profile is functionally matched by cardiovascular correlates, as indicated by the larger ventricles and higher blood hemoglobin concentrations in high-calling rate males. These cardiovascular features are much less developed in females and may result from the fact that females do not engage in vigorous calling behavior. In P. crucifier, a male's calling rate may function as an indicator of the presence of a suite of functionally interrelated traits responsible for the maintenance of this sexually selected display behavior.     

Social signals influence hormones independently of calling behavior in the treefrog (Hyla cinerea)

Social signals play an important role in regulating hormone-behavior relationships. In anurans (frogs and toads), acoustic signals are an essential aspect of reproductive behavior; however, the physiological consequences of receiving social signals has remained largely undescribed. Each night for 5, 10, or 20 days, we presented acoustically isolated male treefrogs with a conspecific mating chorus, an array of tones, or no sound. We recorded calling rate of individuals throughout the experiment and collected blood before and after treatment. Days of stimulus exposure had no effect on any dependent measure. Acoustic treatment influenced steroid levels; testosterone, dihydrotestosterone, and corticosterone increased only in the group exposed to the chorus. Chorus-exposed males also showed an increase in stimulus-evoked calling. We found no correlation between androgens and calling within each treatment group. In addition, noncallers in the chorus group had higher levels of androgens than males in the tone or no sound groups. Further, chorus-exposed males with zero, low, or high rate of calling had similar levels of androgens. These data indicate that social signals increase circulating androgens independently of calling behavior. Elevated corticosterone associated with chorus reception did not inhibit calling behavior, and corticosterone showed no correlation with androgen levels.     

Mating System Variation in Woodhouse's Toad (Bufo woodhousii)

Sexual selection and mating-system variation was studied in two disjunct populations of Woodhouse's toad (Bufo woodhousii) with dissimilar breeding-period durations. In spite of the differences in breeding-period duration, nightly operational sex ratios were roughly equivalent and strongly male biased in both populations, ranging from 0 to 0.5 in the population with a prolonged breeding period, and from 0 to 0.2 in the explosively breeding form. Although operational sex ratios were similar, some males mated with up to three females in the population with an extended breeding period, whereas none of the males mated polygynously in the population with a short breeding season. Two alternative reproductive tactics, satellite and active-searching behavior, were only exhibited by males under high densities in the population with a short breeding period. In the population with an extended breeding period, male mating success was positively related to call rate, but independent of size or number of nights of participation in chorus activity. Although operational sex ratios were equally low, mating was random by size, number of nights of participation in chorus activity, and call rate for males in the explosively breeding population.