Multimodal signals in male European treefrog (Hyla arborea) and the influence of population isolation on signal expression

In nocturnal treefrogs, mate choice implies the use of acoustic and visual signals. Multimodality is suspected to have evolved for either information redundancy or information complementariness. It is essential to explore multimodality in a natural context to understand the selection pressures operating on the signals. In the present study, we investigated calling and coloration in relation to male biometry and condition in four populations of European treefrog (Hyla arborea) varying in size and genetic isolation. We compared the signal intensity between core and satellite populations to estimate the impact of genetic diversity on male secondary sexual traits. The results obtained show important regional variations in both traits, likely as a result of local adaptations. Call and coloration are weakly correlated within an individual, implying that these traits likely convey different information about the signaller's identity or quality, thus supporting the hypothesis of complementariness of multiple messages. By contrast to the experimental evidence, we find that call and coloration are not related to male condition (as estimated by the residual of mass over size), suggesting that the condition‐dependence of these traits may be mediated by complex mechanisms not accurately reflected by the chosen estimator. Finally, male call and colour phenotypes present no robust pattern of variation with isolation status, probably because of variation in local selective pressures and in history of population dynamics. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 633–647.     

Models of female choice in acoustic communication

In this article we present generalized theoretical models ofmate attraction in acoustic communication.The models use simpledecision rules for females and show theoretical differencesbetween the rules in relative attraction of females to soundsources (calling males). The important variables of the modelsare the relative powers of the sources, the distance betweenthe sources and the number of competing signalers.Relative attractionamong sources is a function of their relative power output withmore powerful signals attracting more females. Using differentassumptions about the spacing of sources with respect to femalesensitivity, data from phonotaxis studies can be explained wellby either random pick or active choice models. Bioacousticiansmust reexamine their use of, and conclusions based on, the two-choiceplayback paradigm in studying female mate choice.     

The separate and combined effects of harmonic structure, phase, and FM on female preferences in the barking treefrog (Hyla gratiosa)

In natural advertisement calls of the barking treefrog, Hyla gratiosa, a small amount of incoherent frequency modulation (FM) is present. Incoherency in the FM of a call creates inharmonicity and phase changes between its frequency components. In this study, the combined and separate effects of the harmonic structure, phase spectrum, and FM of an advertisement call on female choice were tested. The harmonic structure of a call can have a direct effect on female preference; females showed a significant preference for static-inharmonic calls over static-harmonic calls. Neither differences in phase or FM alone conferred a preference in two choice tests. However, when FM is present in both calls it does influence female preference for harmonic structure -namely harmonic calls become preferable to inharmonic calls. This reversal of female preference for inharmonicity in a call by the presence of FM suggests that call parameters may interact, and thereby effect mate choice.Abbreviations AP amphibian papilla - BP basilar papilla - FM frequency modulation - PM phase modulation - HS harmonic structure - GB Gaussian Band     

Assessing the potential information content of multicomponent visual signals: a machine learning approach

Careful investigation of the form of animal signals can offer novel insights into their function. Here, we deconstruct the face patterns of a tribe of primates, the guenons (Cercopithecini), and examine the information that is potentially available in the perceptual dimensions of their multicomponent displays. Using standardized colour-calibrated images of guenon faces, we measure variation in appearance both within and between species. Overall face pattern was quantified using the computer vision ‘eigenface’ technique, and eyebrow and nose-spot focal traits were described using computational image segmentation and shape analysis. Discriminant function analyses established whether these perceptual dimensions could be used to reliably classify species identity, individual identity, age and sex, and, if so, identify the dimensions that carry this information. Across the 12 species studied, we found that both overall face pattern and focal trait differences could be used to categorize species and individuals reliably, whereas correct classification of age category and sex was not possible. This pattern makes sense, as guenons often form mixed-species groups in which familiar conspecifics develop complex differentiated social relationships but where the presence of heterospecifics creates hybridization risk. Our approach should be broadly applicable to the investigation of visual signal function across the animal kingdom.     

Traffic noise differentially impacts call types in a Japanese treefrog (Buergeria japonica)

Acoustic noise from automobile traffic impedes communication between signaling animals. To overcome the acoustic interference imposed by anthropogenic noise, species across taxa adjust their signaling behavior to increase signal saliency. As most of the spectral energy of anthropogenic noise is concentrated at low acoustic frequencies, species with lower frequency signals are expected to be more affected. Thus, species with low-frequency signals are under stronger pressure to adjust their signaling behaviors to avoid auditory masking than species with higher frequency signals. Similarly, for a species with multiple types of signals that differ in spectral characteristics, different signal types are expected to be differentially masked. We investigate how the different call types of a Japanese stream breeding treefrog (Buergeria japonica) are affected by automobile traffic noise. Male B. japonica produce two call types that differ in their spectral elements, a Type I call with lower dominant frequency and a Type II call with higher dominant frequency. In response to acoustic playbacks of traffic noise, B. japonica reduced the duration of their Type I calls, but not Type II calls. In addition, B. japonica increased the call effort of their Type I calls and decreased the call effort of their Type II calls. This result contrasts with prior studies in other taxa, which suggest that signalers may switch to higher frequency signal types in response to traffic noise. Furthermore, the increase in Type I call effort was only a short-term response to noise, while reduced Type II call effort persisted after the playbacks had ended. Overall, such differential effects on signal types suggest that some social functions will be disrupted more than others. By considering the effects of anthropogenic noise across multiple signal types, these results provide a more in-depth understanding of the behavioral impacts of anthropogenic noise within a species.     

Interspecific genetics of mate recognition: inheritance of female acoustic preference in Hawaiian crickets

Abstract. Female mating behavior plays a fundamental role in the divergent evolution of mate recognition systems that may lead to speciation. Despite this important role, the phenotypic and genetic bases of female mating behavior remain poorly understood. In this study, I examine the shape of the female acoustic preference function and estimate values for pulse rate preference in two species of Hawaiian crickets, Laupala kohalensis and L. paranigra . In addition, I examine how preference differences are inherited in hybrid crosses between these species. Females expressed unimodal preference functions and were generally more attracted to pulse rates characterizing their own species. Unimodal preference functions also characterized F1 and backcross generations, with hybrid females expressing preferences for intermediate pulse rates. Pulse rate preferences segregated in the backcross generation. Mean pulse rate preference matched mean pulse rate in both parental and hybrid generations. Based on F1 hybrids and segregation patterns in backcross females, I show that changes in both signal and receiver components of the mate recognition system are consistent with a multilocus model of change through incremental steps. The results therefore suggest that ancestors of the current species also expressed unimodal preference functions and that changes in acoustic communication signals occurred through shifts in mean pulse rates and pulse rate preferences among populations.     

The effect of variation in parameters of the male calling song of the katydid,Amblycorypha parvipennis (Orthoptera: Tettigoniidae), on female phonotaxis and phonoresponse

After being placed equidistant from playbacks of two computer-generated male calls, females of the katydidAmblycorypha parvipennis preferentially moved toward call phrases that were louder, longer, and leading (initiated without being overlapped by other call phrase endings). Because earlier tests with calling males had indicated that male mating success was related to these call parameters, we suggest that mating success is partly a result of female choice. Females also preferentially responded to the initial, rather than the latter, half of male phrases. Results of other tests suggested that females were responding to increased phonatome rate characteristic of the first half of the phrase. Males may compete to lead in order to prevent jamming of initial phrase information. Females also preferentially phonoresponded (ticked) in response to longer phrases. In earlier studies of male mating success and female phonotaxis using live males, male weight, sound level, and leading were intercorrelated; however, none of these parameters were correlated with phrase length. We suggest that females may respond to different call parameters under different environmental conditions.     

Heterospecific alarm call recognition in a non-vocal reptile

The ability to recognize and respond to the alarm calls of heterospecifics has previously been described only in species with vocal communication. Here we provide evidence that a non-vocal reptile, the Galápagos marine iguana (Amblyrhynchus cristatus), can eavesdrop on the alarm call of the Galápagos mockingbird (Nesomimus parvulus) and respond with anti-predator behaviour. Eavesdropping on complex heterospecific communications demonstrates a remarkable degree of auditory discrimination in a non-vocal species.     

Choosing a Mate in a Cocktail Party‐Like Situation: The Effect of Call Complexity and Call Timing between Two Rival Males on Female Mating Preferences in the Túngara Frog Physalaemus pustulosus

Signal detection, recognition, and localization are hampered when multiple signalers coincide in time and space, a problem known as ‘cocktail party effect’. In many taxa, senders utter complex calls consisting of two or more elements which often vary in the ease with which they can be assessed in different signaling environments. Receivers’ selective attention to different cues may increase the probability of correctly assigning a signal to its source (localization) in face of conspecific interference. Túngara frogs, Physalaemus pustulosus, produce complex calls consisting of an initial whine, followed by zero up to seven broad‐banded, amplitude‐modulated chucks. Under ideal conditions (without interference or noise), females prefer whines followed by chucks over whines alone, but the preference is not linear; females do not discriminate between whines with one or two chucks. When whines lack chucks, call overlap elicits random responses in females, with no preference for leading calls. In this study, I explored the combined effect of call timing and call complexity on female preferences in a two‐choice paradigm—a simplification of the cocktail party scenario. I tested the hypothesis that the effect of call overlap can be reduced when the calls of one of the two rivals have chucks, specifically more chucks than those of the rival. I gave females a choice between whines alone and with chucks (one or two) presented at three time relations (alternated, abutted, and partially overlapped) and two emission orders (whine with less chucks leading and whine with more chucks leading). I found that the preference for one chuck over no chuck was preserved in all the experimental treatments, but when a w + 2chk preceded a w + chk, either overlapped or abutted, a preference existed for the whine with more chucks. Therefore, an interaction between call order and the number of chucks was obtained. The results only partially supported the hypothesis, and call order emerges as an opportunistic component of signaling in P. pustulosus.     

Cost of sexually embracing a large female offset by the number of eggs fertilized for small male Bufo bufo L.

When pairing with high quality females, a male increases its fitness through an increased number and/or quality of sired offsprings. In anurans, size has often been used as a measure of female quality. In the present study, we examined the effects of pairing with large females for small males in the common toad, Bufo bufo . For the first time in anurans, we show a fitness cost for males to maintain amplexus with a large female. Indeed, although we did not detect any effect of male size on male pairing success in a first breeding event in the presence of other competing males, when males that were successful in the first breeding event were tested for a second time, male pairing success strongly decreased when they had been first paired with a large female. However, the higher fecundity of large females (1.52-fold more than that of small females) may override this pairing cost, especially because high fertilization rate was not linked to male/female body size ratio. Indeed, we did not detect any difference in egg fertilization success between small males paired with large and small females. Our results suggest that predictable cues of female reproductive value exist in common toads, thus meeting a prerequisite of the occurrence of male mate choice. Male mate choice, probably underestimated in anurans, may be particularly important in species where the breeding season is short and the number of mating events for a male is limited. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 755–762.     

Diel variation in a dynamic sexual display and its association with female mate-searching behaviour

Dynamic sexual signals often show a diel rhythm and may vary substantially with time of day. Diel and short-term fluctuations in such sexual signals pose a puzzle for condition capture models of mate choice, which assume a female preference for male traits that reliably reflect a male's quality. Here we experimentally manipulated the food supply of individual male field crickets Gryllus campestris in their natural habitat in two consecutive seasons to determine (i) the effect of male nutritional condition on the fine-scaled variation of diel investment in acoustic signalling and (ii) the temporal association between the diel variation in male signalling and female mate-searching behaviour. Overall food-supplemented males signalled more often, but the effect was only visible during the daytime. In the evening and the night, signal output was still high but the time spent signalling was unrelated to a male's nutritional condition. Females' mate-searching behaviour also showed a diel rhythm with peak activity during the afternoon, when differences among calling males were highest, and where signal output reliably reflects male quality. These findings suggest that males differing in nutritional condition may optimize their investment in signalling in relation to time of day as to maximize mating success.     

Parallel plasticity of mating songs and preferences in the field cricket Gryllus rubens

In animal communication systems, matching mating signals and preferences enable species identification and successful reproduction. In some species, the environment introduces substantial variation in signals and/or preferences. Only a few studies have tested how the match between signals and preferences is maintained despite phenotypic variation. Signal–preference coupling in the context of phenotypic plasticity is the focus of this study. The bivoltine cricket Gryllus rubens displays seasonal differences in the pulse rate of its mating songs. The seasonal effect on other fine‐temporal characters of the songs besides pulse rate, such as pulse and interval duration, duty cycle, as well as the dominant frequency, is not known and is described in the first part of the study for a Kentucky population. In the second part of the study, we tested preferences of spring and fall females to determine whether they match the seasonal plasticity of male songs using single‐speaker phonotaxis experiments. We found that fall songs had a faster pulse rate, shorter pulse and interval durations, and a higher dominant frequency than spring songs. Female preferences shifted in parallel with male song plasticity, that is, spring females preferred the spring song and fall females the fall song. In addition, female responsiveness to male song was plastic as well, that is, fall females were significantly more responsive than spring females. The parallel plasticity of male songs and female preferences facilitates successful communication despite the environmentally induced variation. The potential origin and function of behavioral plasticity in G. rubens are discussed.     

Female large odorous frogs (Odorrana graminea) prefer males with higher nonlinear vocal components

In anurans, the complexity of courtship calls may affect female mate choice. The current study suggests that nonlinear phenomena (NLP) components can contribute to increasing complexity in courtship calls and attracting female attention. The results of a recent study showed that calls of large odorous frog (Odorrana graminea) contained NLP components. However, whether the nonlinear components of courtship calls in O. graminea improve male attractiveness remains unknown. We hypothesized that female O. graminea would prefer males producing calls with a higher proportion of NLP components (P‐NLP‐C). To test this hypothesis, we recorded the advertisement calls of 28 males and confirmed that the P‐NLP‐C was significantly positively related to body size. We also measured the body size of natural amplectant males and non‐amplectant males in the field and found that amplectant males had larger body sizes than non‐amplectant males, and the results of two‐choice amplexus experiments similarly revealed a female preference for males with larger body sizes. Additionally, phonotaxis experiments also revealed that females preferred male calls with a high P‐NLP‐C. The results suggest that a higher P‐NLP‐C in calls can enhance male attractiveness, and the P‐NLP‐C may provide key information about male body conditions for female O. graminea. Our study provides a new insight for better understanding the role of NLP in anuran mate selection.     

Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process

Zebra finches are monogamous birds living in large assemblies, which represent a source of confusion for recognition between mates. Because the members of a pair use distance calls to remain in contact, call-based mate recognition is highly probable in this species. Whereas it had been previously demonstrated in males [Vignal, C., Mathevon, N., Mottin, S., 2004. Audience drives male songbird response to mate's voice. Nature 430, 448-451], call-based mate recognition remained to be shown in females. By analysing the acoustic structure of male calls, we investigated the existence of an individual signature and identified the involved acoustic cues. We tested to see if females can identify their mates on the basis of their calls alone, and performed preliminary experiments using modified signals to investigate the acoustic basis of this recognition. Playback tests carried on six individuals showed that a female zebra finch is able to perform the call-based recognition of its mate. Our experiments suggested that the female uses both the energy spectrum and the frequency modulation of the male signal. More experiments are now needed to decipher precisely which acoustic cues are used by females for recognition.     

Parasites, male-male competition and female mate choice in the sand goby

Male sand goby Pomatoschistus minutus dominance in competition over nest sites was associated with higher body condition but not with the intensity of infection with any individual parasite of six different species, nor with an overall index combining relative levels of infection by all parasites. Body condition was not related to the intensity of infection with any individual parasite nor with the index of total relative parasite load. In trials in which females spawned, they showed a tendency to choose dominant over subordinate males as mates, but did not consistently choose less parasitized males. Variation in the relative size of the dorsal fins of males was detected, and this related to numbers of the ectoparasitic monogenean Gyrodactylus sp., suggesting that at least some infections have phenotypic effects that could allow females to detect and avoid the most heavily infected males.