A mechanism for female choice of large males in the treefrog Hyla chrysoscelis

Summary In this study, we combine both field and laboratory experiments to address the effects of female preference for certain call characteristics on a large-male mating advantage in the treefrog H. chrysoscelis. In laboratory-choice experiments, females always chose the call with the lower fundamental frequency when call rate and call intensity were held constant and the difference in frequency between the two calls was 15%. The lower frequency call was preferred by 8 out of 12 females when the difference in fundamental frequency was 7.4%. These results are consistent with field comparisons of the size of unmated males calling within 2 m of a mated male: Male body size was negatively correlated with fundamental frequency and the greater the size difference, the more likely that the larger male mated. In field choice experiments, females preferred males with higher call rates. Since size differences between males used in this experiment averaged only 2.3 mm, we would not expect the fundamental frequency of a male's call to be the best predictor of mating success. Laboratory results demonstrated that call rate could override female preference for the low frequency call over the high frequency call, while intensity could at least dilute this preference. However, individual males in the field varied both call rate and the call intensity as perceived by the female. We suggest that the interaction between call rate, male size and mating success should be studied further through the use of field-choice experiments.     

Female preferences for spectral call properties in the western genetic lineage of Cope's gray treefrog (Hyla chrysoscelis)

Female frogs discriminate among potential mates based on individual variation in male advertisement calls. While considerable data have accumulated allowing comparisons of female preference functions among species, we still lack fundamental knowledge about how and why the shapes of preference functions for particular call properties vary among populations within all but a few species. Here, we report results from a study aimed at describing female preference functions for spectral call properties in Cope's gray treefrog (Hyla chrysoscelis). Widespread throughout the eastern half of North America, Cope's gray treefrog is the diploid member of the cryptic diploid–tetraploid Hyla versicolor species complex, and its populations are divided into two distinct genetic lineages (eastern and western). In this study of a western lineage population, we recorded and analyzed the spectral properties of 1,000 advertisement calls from 50 males and conducted two-stimulus phonotaxis experiments to estimate a population-level preference function. Females preferred calls with average frequencies over calls with frequencies that were 2 or 3 semitones (1.4 or 2.1 standard deviations, respectively) lower than the population mean. We observed no behavioral discrimination between calls with average and higher-than-average frequencies. Preferences discriminating against low-frequency calls were weak and were abolished by attenuating the preferred average call by 3?dB. We discuss these results in light of previous studies of eastern lineage populations, geographic variation in female preference functions, and the potential adaptive value of discriminating against calls with low frequencies.     

Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments

We studied female mate choice by Hyla versicolor in three venues to examine how acoustic and spatial complexity, background noise, and the calling behavior of males might influence preferences manifest in previous laboratory two-stimulus choice tests. Our laboratory-based two-stimulus choice tests with and without broadcasts of chorus noise demonstrated that females prefer long calls relative to short calls when calling efforts of alternatives are equivalent. Background noise impaired the ability of females to discriminate in favor of longer over shorter calls, but the magnitude of the effect was small. Captures of females at eight speakers broadcasting 6- to 27-pulse calls at the edge of a pond revealed strong discrimination against only the shortest call variant. In natural choruses, females may only rarely encounter males using such unattractive vocalizations. Female phonotaxis at an artificial pond with caged and electronically monitored calling males also indicated that consequences of female preferences for temporal aspects of calling observed in two-stimulus choice tests are much attenuated in choruses and explain only small portions (<10%) of the variation in male mating success. Nevertheless, relatively high call duration and calling effort increased male attractiveness. Acoustic interference emerged as another significant factor influencing male mating success and possibly the differences in female choice observed in laboratory and chorus settings. We suggest that the bias of females against both overlapped and very short calls may help explain why males lengthen their calls but lower their rate of delivery in response to increases in chorus size.     

Interspecific acoustic interactions of the neotropical treefrog Hyla ebraccata

Summary Hyla ebraccata, H. microcephala and H. phlebodes commonly occur together in Panama. The three species have calls exhibiting broad frequency overlap and call during the same season and time of day from similar microhabitats, frequently in close proximity. The vocal repertoires of the three species are structurally and functionally similar. All employ multi-part advertisement and aggressive calls which consist of a primary note followed by a variable number of clicks. H. ebraccata males often responded to heterospecific calls with multi-note synchronized responses, and calls with primary notes greater than 150–200 ms were most effective in eliciting synchrony. Playback experiments with synthetic 1-note advertisement calls of different durations and both synthetic 1-note advertisement calls and 200 ms tones of different frequencies demonstrated that H. ebraccata males will synchronize with stimuli which are similar in frequency and duration to conspecific calls. Data from a two-choice experiment with female H. ebraccata demonstrate that calls of individual H. microcephala can reduce the attractiveness of a H. ebraccata male's calls if primary notes overlap. By synchronizing response calls to those of H. microcephala, a H. ebraccata may reduce the chances that his calls are rendered less attractive to potential mates.Aggressive calls of these species are graded and are characterized by higher pulse repetition rates and often longer durations than advertisement calls. H. ebraccata males respond to aggressive calls of H. microcephala and H. phlebodes as they do to their own calls. Heterospecific aggressive interactions probably occur because the species interfere acoustically. Our results demonstrate that H. ebraccata males behave in ways which enhance their ability to communicate in a noisy assemblage of conspecific and heterospecific males.     

Novel features of an inducible defense system in larval tree frogs (Hyla chrysoscelis)

Organisms in aquatic ecosystems must often tolerate variable environmental conditions, including an uncertain risk of predation. Individuals that can maintain plastic defenses against predation will increase their survival when predators are present, but will not incur the costs of these defenses when the risk of predation is low and the defense is not induced. Larvae of the pond-breeding anuran Hyla chrysoscelis develop a conspicuous phenotype in the presence of predators consisting of a brightly colored tail and a deeper tail fin. In this study, I attempted to identify the source of the chemical signal that induces this defensive morphology in this species. I tested whether metabolites alone, originating from the prey but passing through the predator, were able to induce the same morphological response as the combination of alarm signals released directly by attacked conspecifics, and metabolites. I used morphometric and tail conspicuousness data to assess tadpole response to the perceived risk of predation by larval odonate predators (Anax junius). I also tested whether this inducing cue could be recognized across species by measuring the morphological response of H. chrysoscelis tadpoles exposed to cues emitted when tadpoles of a closely related genus (Pseudacris crucifer) were consumed. Tadpoles exhibited a clean graded response of both overall shape and tail morphology in response to all cues, corresponding to their relative reliability as indicators of a risk of predation. H. chrysoscelis tadpoles were also able to respond to cues emitted when tadpoles of a closely related genus were consumed by predators. These results illustrate that tadpoles of this species are able to respond to metabolites alone without alarm signals, and that interspecific chemical communication is a primary mechanism for predator avoidance in this inducible defense system.     

Carbohydrate and calling: Depletion of muscle glycogen and the chorusing dynamics of the neotropical treefrog Hyla microcephala

Chorusing males of the neotropical treefrog Hyla microcephala call in distinct bouts punctuated by periods of silence, a pattern known as unison bout singing. Schwartz (1991) previously tested and refuted the hypotheses that males periodically stop calling either because of a female preference for males that call cyclically, or because high ambient noise levels inhibit vocal activity. Males of H. microcephala are vocally responsive to the calls of other males, and during calling bouts their rate of note production can exceed 10,000 per hour. In natural choruses females preferentially pair with males that call at the higher rates. Because females can pair with males over many hours, males may stop calling periodically to save energy so they can continue to call for the entire period that females are available. We directly tested this energy conservation hypothesis by collecting samples of males early in the evening just after chorusing commenced and later when chorusing had ended for the night. Trunk muscles (internal and external oblique), which are responsible for the airflow associated with note production, were dissected, frozen, and their glycogen content measured. Data on calling behavior were obtained for late-evening samples. Individual calling behavior was not correlated with a males final glycogen level. In addition, many males ended their calling before glycogen reserves were exhausted, indicating that factors other than energy can determine when males finally stop chorusing, However, the biochemical assays supported the energy conservation hypothesis. Unless chorusing was punctuated by pauses, most males would have been unable to sustain high rates of calling for an entire evening without exhausting glycogen reserves in their trunk muscles. Because the time females pair with males is probably unpredictable to males, the ability to call for long periods may improve a males chances of mating.     

The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor)

Summary The vocal behavior of Hyla versicolor was studied in the field by means of behavioral observations and playback experiments, and these data were coupled with measurements of oxygen consumption in calling frogs to estimate the effect of social interactions on calling energetics. Male gray treefrogs have intense calls (median peak SPL=109 dB, fast RMS SPL=100 dB at 50 cm). At an air temperature of 23° C, males produced an average of 1,200–1,300 calls/h for 2–4 h per night. Calling rates and call durations differed among individuals, but were relatively constant for each male during periods of sustained calling. Males in dense choruses gave calls about twice as long as isolated males, but produced calls at about half the rate. Consequently, total calling effort and estimated aerobic costs were largely independent of chorus density. Playbacks of recorded calls to males in the field elicited increases in call duration and decreases in calling rate, regardless of the rate or duration of the stimulus. Males gave longer calls in response to long calls or to stimuli presented at high rates, but they did not precisely match either stimulus rate or duration. Calling effort and estimated oxygen consumption changed only slightly during stimulus playbacks. These results indicate that male-male competition elicits pro-found changes in the vocal behavior of calling males, but these changes have little effect on energy expenditure. We estimated that most calling males had metabolic rates of about 1.7–1.8 ml O₂/(g\h), or about 280 J/h for an average size (8.6 g) male at 20° C. Although changes in call duration and calling rate did not affect aerobic costs of calling, males producing long calls at slow rates called for fewer hours per night than males producing shorter calls at higher rates. This suggests that calling time may be limited by the rate at which muscle glycogen reserves are depleted.     

Female preferences for multiple attributes in the acoustic signals of the Italian treefrog, <Emphasis Type="Italic">Hyla intermedia</Emphasis>

The advertisement call of frogs and toads is an example of multiple message signal because different acoustic properties encode different kinds of biologically significant information. In the Italian treefrog, Hyla intermedia, pulse rate and frequency have been found to be under stabilizing female preferences and to encode information important for mate recognition, whereas the number of calls per call group have been found to be under directional preferences and, thus, to be important for mate quality assessment. In this study, we investigate preferences for calls that differ simultaneously in frequency, pulse rate, and number of calls per call group, and we ask how these properties interact with each other in influencing female mating decisions. Results of two-choice phonotaxis experiments provide no evidence to support the hypothesis that females process multi-attribute signals in a hierarchical way. In contrast, the pattern of preferences is consistent with the ‘preference function’ hypothesis, that is, with the hypothesis that females rank signals along an ordinal scale of values and choose accordingly. Pulse rate and frequency influence mating preferences more than does the number of calls per call group. The interaction between pulse rate and frequency is not additive but multiplicative: small differences in either pulse rate or frequency that, alone, have no effects on female choice, interact synergistically so that their combination has strong influence on female preferences. A preference repeatability test shows strong among-female differences in preference for multi-attribute signals. We suggest that this result reveals not only a variation in attribute values among females, but also a variation in the way females weight and combine attribute values into a single preference score.     

Male calling behavior,female discrimination and acoustic interference in the Neotropical treefrog Hyla microcephala under realistic acoustic conditions

Summary Anuran choruses are acoustically complex assemblages of calling males. Little is known about the behavior of males or females in such natural sound environments. I studied calling behavior of males of Hyla microcephala in nature by using an interactive computer-based system that allowed me to simulate call interruptions by a number of males. I also monitored the calling behavior of groups of four to six males. When a male is interrupted by the call of another frog, he increases the spacing between the notes of his call. Responses of this kind are strongest to the loudest neighbor, and some males may ignore interruptions by all but a single close male. Interruptions using synthetic calls with silent gaps indicated that males respond vocally to reductions in sound intensity as brief as 20 ms. This ability helps to explain how males can rapidly alternate notes during pairwise interactions. Amounts of acoustic overlap between pairs of males in the choruses were usually below 10% of an individual's total calling time during bouts. The time a male spent calling that was free of acoustic interference by any other male ranged from 34–92% of his total calling time. When group size was decreased, this unobstructed calling time increased. Previous research showed that females of H. microcephala discriminate against calls that overlap so that the call pulse-train structure is degraded. Here I show that a 6 dB difference in intensity between the overlapped calls is sufficient to reduce the degradative effect of call interference. Females were also given a choice between interfering calls broadcast from two adjacent and two widely separated speakers. An angular separation between speakers of 120° was insufficient to elicit a preference for the separated sources. Together, data on behavior of males and females indicated that males actively reduce acoustic interference with those loud individuals most likely to degrade seriously the temporal structure of their calls.     

Interactions in male baboons: the importance of both males’ testosterone

To date, research on testosterone and behavior has focused on individuals, even when studying social behaviors that necessarily involve multiple participants. Here, we explore male responses to other males of different dominance ranks and testosterone levels in a population of wild baboons. In chacma baboons (Papio hamadryas ursinus) of the Okavango Delta, a male’s testosterone is related to his rank trajectory and, therefore, the threat he poses to other males. To examine the effects of testosterone and rank on male–male interactions, we used playback experiments to measure how a target male responded to the simulated approach of another male, scoring responses by whether or not the subject moved away from the speaker in the first minute. High testosterone subjects did not move away from the speaker more often than low testosterone subjects, but high testosterone callers elicited a move more often than low testosterone callers. When the combined testosterone of the subject and caller was high, moves were most common. The rank relationship between subject and caller did not predict moves, but the effect of combined testosterone on moving was most pronounced in adjacently ranked males. Adjacently ranked, high testosterone males are the most likely to be competing for each others’ rank, and our experiments on these dyads elicited the most moves. Both behavioral and experimental observations indicate that testosterone may be more important than the rank relationship in predicting the outcome of male–male interactions. Furthermore, combined information on the testosterone of both males was the best predictor of results, highlighting the utility of dyadic analyses when relating testosterone to behavior.     

Alternative mating tactics in the Italian treefrog, <Emphasis Type="Italic">Hyla intermedia</Emphasis>

As in many lekking anurans, Italian treefrog males use two mating tactics: they can attract females by calling vigorously or be satellites, that is, they can remain silent in proximity of a calling male and try to intercept females attracted by their neighbour. We investigated the factors that affected the expression of this mating tactic. Consistent with the conditional mating tactic hypothesis, satellites were smaller than average and smaller than their parasitised calling males. They spent a larger-than-average number of nights at the breeding site, where most of them were also observed calling. Moreover, satellites showed lower call rates and lower mating success than those of males they parasitise but not lower than those of males they did not parasitise. Overall, these results, together with those derived from the analyses of the seasonal and spatial distribution of males, provide evidence for a non-random association between satellites and calling males and are consistent with the hypothesis that satellites have spectral and temporal acoustic preferences that parallel those of females. By adopting the less-successful satellite mating tactic, competitively inferior males can nevertheless maximise their potential reproductive fitness by sexually parasitising the most attractive chorusing males.     

Female mate choice in the Pied Flycatcher Ficedula hypoleuca

Summary We have examined male and territorial factors which might influence female mate choice in the Pied Flycatcher (Ficedula hypoleuca). Mating success of males was largely determined by the order of arrival on the breeding grounds. Females actively selected those males that had been longest in the area. This is likely to be due to territorial cues, early males having the best territories. About 15% of the males become polygynous, and these are the males that arrived earliest.Male age was relatively unimportant for breeding success, but because old males tend to arrive earlier than yearlings, most polygynous males were old. On average, old males are somewhat darker than young males, but male colour also varies within males of the same age. Polygynous and monogamous males did not differ significantly in colour, and female breeding success was not correlated with the colour of their mates. We show theoretically that it does not pay for females to select young males to avoid polygyny unless polygyny frequency or the number of reliable monogamous males almost double. Hence our hypothesis of polygyny-by-deceit in the Pied Flycatcher remains realistic. Because of male polyterritoriality, females are unaware of the males' status when mating.     

Female choice in sage grouse: the roles of attraction and active comparison

Previous studies of female choice in sage grouse Centrocercus urophasianus have implicated both the acoustic quality and repetition rate of the stereotyped strut display as putative cues for female choice. Stages in the choice process at which specific components of male courtship display influence female decisions were investigated using field observations of female pre-mating behavior. Females visited a subset of territorial males and then actively chose one of these as a mate. The order in which males were visited suggested that females searched until an acceptable mate was found, rather than employing a “best-of-n” tactic. Numbers of females visiting a male were related to differences in an acoustical component of display (inter-pop interval) whereas the probability that a visiting female mated was related to display rate (Table 3), indicating that initial attraction and active choice are influenced by different components of display. In addition, inter-pop interval and display rate tended to covary inversely (Fig. 1), suggesting that attraction and active choice may impose conflicting selection pressures on display performance. Received: 11 November 1995/Accepted after revision: 16 March 1996     

Female choice for complex song in the European starling: a field experiment

Male European starlings Sturnus vulgaris sing long complex songs that appear to be important in the courtship of females but which also influence competitive interactions between males. We tested the hypothesis that females choose mates on the basis of the complexity of their songs, rather than on the quality of the territories the males defended. In order to determine whether certain territories were preferred over others, the first set of birds to settle in the experimental nest-boxes was removed and a second set allowed to settle. Consistent preferences for certain nest-boxes were indicated by correlations between the settlement patterns of the first and second sets of birds. However, males with the most complex song did not necessarily occupy the most preferred nest sites. Males with more complex song acquired mates faster. This relationship remained significant when nest-site preference was statistically controlled, indicating that female starlings chose males with complex song rather than those that defended preferred nest sites. A number of morphological variables were also found to be uncorrelated with female choice. Song complexity in European starlings increases with age, and the evolution of song complexity in this species is consistent with an age-indicator model of sexual selection. Males with larger repertoires were also in better condition, indicating that females obtain high-quality mates by choosing on the basis of male song. Received: 29 April 1995/Accepted after revision: 9 September 1995     

Consensus among females in their choice of males in the guppy Poecilia reticulata

We studied female guppies from two populations (Trinidad and Jemez Springs, New Mexico) to determine their mating preferences, the degree of consensus among females for particular male phenotypes, and the variation among females for the types of traits they prefer. We recorded the visual responses of 68 Trinidad and 10 Jemez females in paired male trials. The three sexually-selected male traits quantified were the area of orange color and iridescence on the body, and display behavior. Females from the Trinidad population agreed in their choice of males in three of the eight replicates, and this agreement was based on display rate rather than male color patterns. Females from the Jemez population showed no agreement in their preferences of males. Mating preferences of females varied both between populations and among females of a population. In both populations, female preferences were based primarily on courtship intensity and only secondarily on color pattern. However, females from both populations differed in the relative importance of orange color and iridescence. The fact that females differ in criteria for evaluating males has important implications for selection and maintenance of color polymorphisms and for the interactions among multiple secondary sexual traits of males in the guppy. Received: 5 December 1995/Accepted after revision: 7 June 1996     

Female mate selection in the natterjack toad: active choice or passive atraction?

Summary Variation in seasonal mating success among male natterjack toads (Bufo calamita) was influenced by the number of nights that males spent at the pond and by male body size. Large males produced louder and lower frequency calls than small males, and maintained larger acoustic territories. After arriving at the pond, one half of all observed females mated with the first male they encountered. The remainder visited several males before initiating amplexus, but no criteria could be identified that females might have used when deciding whether to accept or reject a male. Movements between several males seem to be best explained by low female responsiveness to male advertisement calls on cold nights which were nonoptimal for oviposition. Females attempted to reject non-calling males both before and after amplexus, but this may be a mechanism to avoid mismating with males of the common toad (Bufo bufo), an explosive breeder that utilised the same pond. In two-choice playback experiments using synthetic advertisement calls, females showed no preference for calls based on their frequency. Females preferred calls of intermediate pulse repetition rate equivalent to those produced by a male at the same body temperature. Pulse rate is thus potentially subject to stabilishing selection and may be an important character for species-recognition. Females preferred fast rather than slow call rates, but only when the alternative rates were extreme. They also preferred calls which they perceived at the highest sound pressure level, but did not discriminate between absolute sound pressure levels of alternative stimuli at different distances. Since females that delay mating and oviposition may suffer predation, it is suggested that female preference for loud, rapidly repeated calls may be adaptive in the sense of minimizing the costs of locating conspecific males, rather than maximizing the probability of obtaining a high quality mate. Competition between males to maintain large acoustic territories and produce calls that can be easily detected by females would seem to be a sufficient mechanism to explain the evolution of the striking calls produced by male natterjacks.     

Advertisement-call modification,male competition,and female preference in the bird-voiced treefrog <Emphasis Type="Italic">Hyla avivoca</Emphasis>

Senders and receivers influence dynamic characteristics of the signals used for mate attraction over different time scales. On a moment-to-moment basis, interactions among senders competing for a mate influence dynamic characteristics, whereas the preferences of receivers of the opposite gender exert an influence over evolutionary time. We observed and recorded the calling patterns of the bird-voiced treefrog Hyla avivoca to assess how the dynamic characters of calls vary during interactions among groups of males in a chorus. This question was also addressed using playback experiments with males. Playback experiments with females showed how changes in dynamic call properties are likely to affect male mating success. Frogs calling in pairs, groups, or in response to playbacks produced longer calls than did isolated males. During call overlap, males often increased the duration of the silent interval (gaps) between the pulses of their calls so that the pulses of the calls of two neighbors interdigitated. This change resulted in increased variability of pulse rate, a traditionally static acoustic property; however, males also produced high proportions of non-overlapped calls in which variability in pulse rate was low and had species-typical values. Females preferred long calls to short- and average-duration calls, and non-overlapped calls to overlapped calls. Given a choice between pairs of overlapped calls, females preferred pairs in which the proportion of overlap was low and pairs in which the pulses of such calls interdigitated completely. The observed patterns of vocal competition thus reflect the preferences of conspecific females, which have influenced the evolution of the calling behavior of H. avivoca. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.