Calling Effort Research Articles

Listening to male song induces female field crickets to differentially allocate reproductive resources

Differential investment in offspring by mothers is predicted when there is substantial variation in sire quality. Whether females invest more resources in the offspring of high-quality mates (differential allocation, DA) or in the offspring of low-quality mates (reproductive compensation, RC) is not consistent in the literature and both effects can be predicted by theoretical models. In the field cricket, Grylluspennsylvanicus Burmeister, 1838 (Orthoptera: Gryllidae: Gryllinae), females are attracted more to calling songs of high-quality males than to those of low-quality males. We tested whether females invest reproductive resources differentially based on perceived mate quality. We manipulated female perception of male quality by allowing virgin females to approach a speaker broadcasting either high- or low-quality calling song (high or low calling effort respectively), and then mated them with a randomly chosen male that had been rendered incapable of calling. In the week following mating, females exposed to high-quality calling song gained less weight, laid more embryos, and laid larger embryos than females exposed to low-quality calling song, although only the first of these effects was statistically significant. These results support the DA hypothesis and suggest that females invest their reproductive output based on a trait (calling effort) that is an honest indicator of male quality.

Behavioral, physiological and morphological correlates of parasite intensity in the wild Cururu toad (Rhinella icterica).

Large numbers of parasites are found in various organs of anuran amphibians, with parasite intensities thought to modulate the host's Darwinian fitness traits. Interaction between the anuran hosts and their multiple parasites should modulate the host's phenotypic characteristic, such as those associated with high energetic demand (such as calling effort and locomotor performance), energy balance (standard metabolic rate), and morphological plasticity (as indicated by organ masses). The present study investigated the impact of parasite intensities on the behavioral, physiological, and morphological traits of wild adult male Rhinella icterica (Anura: Bufonidae). We tested as to whether individuals with higher parasite intensities would present: 1) lower vocal calling effort in the field, as well as poorer locomotor performance and body-condition index; and 2) higher standard metabolic rates and internal organ masses. Measurements included: calling effort in the field; standard metabolic rate; locomotor performance; parasite intensity; internal organ masses (heart, liver, kidneys, intestines, stomach, lungs, hind limb muscle, and spleen); and the body-condition index. Results showed a negative association of parasite intensities with locomotor performance, and standard metabolic rate of R. icterica. A positive association between parasite intensities and relative organ masses (heart, intestines and kidneys) was also evident. Toads with higher pulmonary and intestinal parasites intensities also showed higher total parasite intensities.

Male–male interactions and male mating success in the leafhopper Aphrodes makarovi

AbstractIn mating systems based on substrate‐borne vibrations, sexual communication often involves a reciprocal exchange of species‐ and sex‐specific vibrational signals and male is searching for a stationary female. In the leafhopper Aphrodes makarovi, female reply is essential for successful location of the female and its variable duration directly affects male's costs associated with signalling and searching. We studied male and female behaviour in a trio situation (two males and one female), and our results show that male–male competition had important effects on male mating success. Females replied equally to advertisement calls emitted by the winning and losing males and mated with the first male that located them, regardless of his investment in calling effort. Males eavesdropped to male–female duet maintained by the rival, and the winners were better at exploiting female replies to the rival's advertisement calls by silently approaching the female. To interfere with the ongoing male–female duet, males also emitted masking signals overlapping the latter part of the female reply. More overlapped female replies were registered in response to the losers and masking signals most likely delay the rival in reaching the female. Our study shows that a comprehensive understanding of male mating success and female preferences in vibrational duetting systems requires also investigations in more complex settings that more realistically represent the situation in nature.

The metabolic costs of sexual signalling in the chirping katydid Plangia graminea (Serville) (Orthoptera: Tettigoniidae) are context dependent: cumulative costs add up fast.

Katydids produce acoustic signals via stridulation, which they use to attract conspecific females for mating. However, direct estimates of the metabolic costs of calling to date have produced diverse cost estimates and are limited to only a handful of insect species. Therefore, in this study, we investigated the metabolic cost of calling in an unstudied sub-Saharan katydid, Plangia graminea Using wild-caught animals, we measured katydid metabolic rate using standard flow-through respirometry while simultaneously recording the number of calls produced. Overall, the metabolic rate during calling in P. graminea males was 60% higher than the resting metabolic rate (0.443±0.056 versus 0.279±0.028mlCO2h-1 g-1), although this was highly variable among individuals. Although individual call costs were relatively inexpensive (ranging from 0.02 to 5.4% increase in metabolic rate per call), the individuals with cheaper calls called more often and for longer than those with expensive calls, resulting in the former group having significantly greater cumulative costs over a standard amount of time (9.5 h). However, the metabolic costs of calling are context dependent because the amount of time spent calling greatly influenced these costs in our trials. A power law function described this relationship between cumulative cost (y) and percentage increase per call (x) (y=130.21x-1.068, R2=0.858). The choice of metric employed for estimating energy costs (i.e. how costs are expressed) also affects the outcome and any interpretation of costs of sexual signalling. For example, the absolute, relative and cumulative metabolic costs of calling yielded strongly divergent estimates, and any fitness implications depend on the organism's energy budget and the potential trade-offs in allocation of resources that are made as a direct consequence of increased calling effort.

Field Crickets Compensate for Unattractive Static Long-Distance Call Components by Increasing Dynamic Signalling Effort.

The evolution of multiple sexual signals presents a dilemma since individuals selecting a mate should pay attention to the most honest signal and ignore the rest; however, multiple signals may evolve if, together, they provide more information to the receiver than either one would alone. Static and dynamic signals, for instance, can act as multiple messages, providing information on different aspects of signaller quality that reflect condition at different time scales. While the nature of static signals makes them difficult or impossible for individuals to augment, dynamic signals are much more susceptible to temporary fluctuations in effort. We investigated whether male Texas field crickets, Gryllus texensis, that produce unattractive static signals compensate by dynamically increasing their calling effort. Our findings lend partial support to the compensation hypothesis, as males that called at unattractive carrier frequencies (a static trait) spent more time calling each night (a dynamic trait). Interestingly, this finding was most pronounced in males that called with attractive pulse characteristics (static traits) but did not occur in males that called with unattractive pulse characteristics. Males that signalled with unattractive pulse characteristics (duration and pause) spent less time calling through the night. Our correlative findings on wild caught males suggest that only males that signal with attractive pulse characteristics may be able to afford to pay the costs of both trait exaggeration and increased calling effort to compensate for poor carrier frequencies.

Spatio-Temporal Dynamics of Field Cricket Calling Behaviour: Implications for Female Mate Search and Mate Choice.

Amount of calling activity (calling effort) is a strong determinant of male mating success in species such as orthopterans and anurans that use acoustic communication in the context of mating behaviour. While many studies in crickets have investigated the determinants of calling effort, patterns of variability in male calling effort in natural choruses remain largely unexplored. Within-individual variability in calling activity across multiple nights of calling can influence female mate search and mate choice strategies. Moreover, calling site fidelity across multiple nights of calling can also affect the female mate sampling strategy. We therefore investigated the spatio-temporal dynamics of acoustic signaling behaviour in a wild population of the field cricket species Plebeiogryllus guttiventris. We first studied the consistency of calling activity by quantifying variation in male calling effort across multiple nights of calling using repeatability analysis. Callers were inconsistent in their calling effort across nights and did not optimize nightly calling effort to increase their total number of nights spent calling. We also estimated calling site fidelity of males across multiple nights by quantifying movement of callers. Callers frequently changed their calling sites across calling nights with substantial displacement but without any significant directionality. Finally, we investigated trade-offs between within-night calling effort and energetically expensive calling song features such as call intensity and chirp rate. Calling effort was not correlated with any of the calling song features, suggesting that energetically expensive song features do not constrain male calling effort. The two key features of signaling behaviour, calling effort and call intensity, which determine the duration and spatial coverage of the sexual signal, are therefore uncorrelated and function independently.

Robust calling performance in frogs infected by a deadly fungal pathogen.

Reproduction is an energetically costly behavior for many organisms, including species with mating systems in which males call to attract females. In these species, calling males can often attract more females by displaying more often, with higher intensity, or at certain frequencies. Male frogs attract females almost exclusively by calling, and we know little about how pathogens, including the globally devastating fungus, Batrachochytrium dendrobatidis, influence calling effort and call traits. A previous study demonstrated that the nightly probability of calling by male treefrogs, Litoria rheocola, is elevated when they are in good body condition and are infected by B. dendrobatidis. This suggests that infections may cause males to increase their present investment in mate attraction to compensate for potential decreases in future reproduction. However, if infection by B. dendrobatidis decreases the attractiveness of their calls, infected males might experience decreased reproductive success despite increases in calling effort. We examined whether calls emitted by L. rheocola infected by B. dendrobatidis differed from those of uninfected individuals in duration, pulse rate, dominant frequency, call rate, or intercall interval, the attributes commonly linked to mate choice. We found no effects of fungal infection status or infection intensity on any call attribute. Our results indicate that infected males produce calls similar in all the qualities we measured to those of uninfected males. It is therefore likely that the calls of infected and uninfected males should be equally attractive to females. The increased nightly probability of calling previously demonstrated for infected males in good condition may therefore lead to greater reproductive success than that of uninfected males. This could reduce the effectiveness of natural selection for resistance to infection, but could increase the effectiveness of selection for infection tolerance, the ability to limit the harm caused by infection, such as reductions in body condition.

Calling rate, corticosterone plasma levels and immunocompetence of Hypsiboas albopunctatus

During the breeding season, male anuran amphibians produce advertisement calls. Androgens play a permissive role in the activation of calling activity, which is often positively correlated to androgen plasma levels and testes mass. Additionally, calling effort is also correlated to corticosterone plasma levels (hereinafter referred to as CORT), which is associated with the mobilization of energy substrates to sustain the high energy flux associated with this activity. However, high CORT also has many immunosuppressive effects and might interfere with reproduction. Consequently, CORT might mediate a compromise between reproductive effort and immunocompetence in anurans. In the present study, we investigated the relationship between calling rate, immunocompetence, and CORT in Hypsiboas albopunctatus, a midsize anuran occurring in South America. To understand these relationships, we conducted focal observations of calling behavior, followed by blood collection for CORT measurements and evaluation of some immune parameters. Our results showed that individuals with larger testes had higher calling rates, and those with higher calling rates showed lower cell-mediated immune response (swelling response to phytohaemagglutinin), although these relationships were not mediated by CORT. Furthermore, males calling early in the evening showed high CORT, and individuals with lower body condition index had higher CORT. We conclude that calling activity shows a cost in terms of cellular immune response in H. albopunctatus, but this compromise does not appear to be mediated by glucocorticoid plasma levels.

Are simakobu (Simias concolor) loud calls energetically costly signals?

Male vocal displays play an important role in sexual selection in many species. If there are costs or constraints, calls may convey honest information about the caller. We studied the loud calls of male simakobu (Simias concolor), a sexually dimorphic primate that resides in one-male groups, on Siberut Island, Indonesia. We combined behavioral and ecological data with acoustic analysis to determine the influence of energy costs and status on calling effort. Based on all-day follows (n = 107) and loud-call recordings (n = 186), we determined how calling rates and durations varied in relation to short-term (time of day, temperature, travel distance) and long-term (fruit availability, physical condition) measures of energy availability and expenditure. We found that males avoided calling at the hottest times of the day, and produced shorter calls at higher temperatures, supporting the hypothesis that calls are influenced by thermoregulation costs. A peak of longer duration calls just before sunrise, however, could not be explained by energy constraints, but we hypothesize that this pattern is related to the fact that dawn calls occur in choruses, motivating males to call longer than their neighbors. Contrary to predictions, calling rates increased with decreasing fruit availability and did not appear to be energetically costly. We hypothesize that calling rates instead reflect strategies involving feeding and/or mate competition, signaling the motivation, rather than fighting ability, of the caller. Overall, results only weakly support the hypothesis that the timing and duration-but not rate-of simakobu loud calls are influenced by energy costs. Am J Phys Anthropol 161:44-52, 2016. © 2016 Wiley Periodicals, Inc.

Sender–receiver dynamics in leafhopper vibrational duetting

A coordinated reciprocal exchange of acoustic signals (duetting) is common in arthropods relying on substrate-borne vibrational signalling. Communication between partners is under evolutionary pressures resulting from ecological and sexual selection and reciprocal effects arising from such dynamic interactions may influence the sender's and receiver's mating success. We investigated the influence of female reply duration on male mate-searching effort in the leafhopper Aphrodes makarovi in which the female reply is essential for successful location of the female. In a duet, the beginning of a female reply overlaps the end of the male call and males evaluate only the nonoverlapped duration of the female reply. In playback experiments we varied the duration of female replies within the natural range. The duration of a female reply was negatively correlated with the male calling effort. By increasing her reply duration a female may significantly reduce the male's direct and indirect costs associated with signalling and searching, thus, ultimately, affecting male reproductive success. Males showed high adaptability in signalling behaviour and when female replies were short, searching males shortened the last section of their advertisement calls. This strategy allows the nonoverlapped part of the female reply to be longer irrespective of its overall duration. Despite its deceptively simple form, vibrational duetting may entail more complex interactions than just temporal coordination.

Age-dependent pattern of calling behavior in Atheloca subrufella (Hulst) (Lepidoptera: Phycitidae)

Changes in the signaling effort of virgin females are known to occur until their first mating. Young females tend to increase the calling effort (number and time duration of bouts) as they age. In this context, the calling behavior of virgin females of Atheloca subrufella, an important pest of coconut palms (Cocos nucifera), was studied under laboratory conditions. Thirty four virgin females were observed during 16 scotophases (25 ± 2 °C, 75 ± 5 % RH and 10 h scotophase), until they stopped calling in the following photophase. The calling position, pattern and frequency were evaluated. Females of A. subrufella showed only one calling position, and calling peaked between the second and fifth scotophases. Most females did not start calling immediately after emergence. Neither the individual duration of calling nor the number of calling bouts changed over time. However, the time that calling started was earlier in older females, probably to avoid competition with younger females and increase the probability of mating. These data support the hypothesis that there is an age-dependent pattern of pheromone emission in virgin females of A. subrufella.

Breeding under unpredictable conditions: Annual variation in gonadal maturation, energetic reserves and plasma levels of androgens and corticosterone in anurans from the Brazilian semi-arid

Anurans living in arid and semi-arid habitats are subjected to unpredictable rain patterns. Consequently, they should be prepared to reproduce at the onset of rain events. We investigated the covariation between calling behavior, testicular maturation, abdominal fat body index (FBI), plasma levels of androgens (T-DHT) and corticosterone (CORT) of males from three species of anurans in the Brazilian semi-arid during the reproductive period and drought. One of these species aestivates during the drought, while the other two species remain foraging. Although the three species display different behavioral strategies during the dry period, they present the same general reproductive patterns. T-DHT levels on the plasma and germinative cyst diameters were higher during the reproductive and breeding period compared to the drought. Additionally, the germinative cysts had all cell stages including sperm bundles during the dry season, however, it was only during the breeding event that free spermatozoa were found in the cyst lumen. These results suggest that these species present the reproductive pattern typical of desert anurans, consisting of opportunistic breeders that reproduce when triggered by a rain stimulus. Rhinella jimi and Pleurodema diplolister had higher CORT when males were calling. Moreover, Rhinella granulosa and P. diplolister showed lower FBI during breeding event, when males were calling. The high levels of CORT and lower FBI during reproductive period are associated, indicating that CORT modulates the recruitment of energy stores to prepare and maintain reproduction, particularly the expensive calling effort.

Male treefrogs in low condition resume signaling faster following simulated predator attack

Current models indicate that an organism’s sensitivity to risk may be heavily influenced by the trade-off between current and future reproduction. Individuals that have fewer future reproductive opportunities are expected to show more risky behavior as they have less to lose if captured by a predator (the asset protection principle). In this study, we examined the effects of age and physical condition on risk taking behavior during sexual signaling in the gray treefrog (Hyla versicolor) to test the prediction that older and poor condition males will take greater risks than their younger or higher-condition counterparts. In accordance with these predictions, we found that males in low physical condition resumed signaling activity more rapidly following a simulated predator attack than their higher-condition counterparts, although this effect was only apparent in one of two study years. Further, males that resumed calling early did not offset their risk of detection by predators via reduced calling effort. Contrary to our predictions, we did not find age to be a significant predictor of risk taking in male signaling behavior. We conclude with a discussion of possible explanations for the discrepancy observed between years and highlight the potential reproductive consequences of variation in risk taking behavior.

Age related decline in female lar gibbon great call performance suggests that call features correlate with physical condition.

BackgroundWhite-handed gibbons (Hylobates lar) are small Asian apes known for living in stable territories and producing loud, elaborate vocalizations (songs), often in well-coordinated male/female duets. The female great call, the most conspicuous phrase of the repertoire, has been hypothesized to function in intra-sexual territorial defense. We therefore predicted that characteristics of the great call would correlate with a caller’s physical condition, and thus might honestly reflect resource holding potential (RHP). Because measurement of RHP is virtually impossible for wild animals, we used age as a proxy, hypothesizing that great call climaxes are difficult to produce and maintain over time, and that older adults will therefore perform lower quality great calls than young adults. To test this we analyzed the great call climaxes of 15 wild lar gibbon females at Khao Yai National Park, Thailand and 2 captive females at Leo Conservation Center, Greenwich, CT.ResultsFindings show that call climaxes correlate with female age, as young animals (n = 8, mean age: 12.9 years) produced climaxes with a higher frequency range (delta F0), maximum F0 frequency and duty cycle than old animals (n = 9, mean age: 29.6 years). A permuted discriminant function analysis also correctly classified calls by age group. During long song bouts the maximum F0 frequency of great call climaxes’ also decreased. Additional data support the hypothesis that short high notes, associated with rapid inhalation as an individual catches its breath, reflect increased caller effort. Older females produced more high notes than younger females, but the difference only approached statistical significance, suggesting that calling effort may be similar across different ages. Finally, for the first time in this species, we measured peak intensity of calls in captive females. They were capable of producing climaxes in excess of 100 dB at close range (2.7 m).ConclusionsAge and within-bout differences in the lar gibbon great call climax suggest that call features correlate with physical condition and thus the call may have evolved as an honest signal in the context of intra-sexual territorial defense and possibly also in male mate choice via sexual selection, although further testing of these hypotheses is necessary.

Attendance, but not performance, predicts good genes in a lek-breeding treefrog

According to the good-genes hypothesis, females prefer males with costly displays because the costs are reliable indicators of genetic quality. In leks, mating costs result from a multiplicative interaction between the number of display performances (lek attendance) and the energetic expenditure associated with each display performance. If males differ in their allocation strategies between the 2 components of mating effort, the reliability of display performance as an indicator of genetic quality may be disrupted. Here, we investigate the association between male genetic quality and both lek attendance and display performance in the Italian treefrog, Hyla intermedia. We recorded lek attendance and display performance (nightly calling effort) during 2 breeding seasons, and we set up a breeding experiment to evaluate sire effects on 3 larval fitness-related traits (growth rate, age, and size at metamorphosis). Attendance and calling effort were positively correlated with each other and both with male mating success, providing no evidence for a performance-attendance trade-off at the population level. In the breeding experiment, we found some evidence for an effect of sire identity and attendance on growth rate and age at metamorphosis, but no evidence for an effect of sire calling effort. We conclude that female preference, by imposing high-quality standards for calling males, strengthens the role of endurance rivalry in male mating competition, indirectly favoring males of higher-than-average mating effort. Under this scenario, although male displays are unreliable indicators of mating quality, females nevertheless gain benefits because of the reduced risk of coming on low-quality males.

Are attractive male crickets better able to pay the costs of an immune challenge?

Reproduction and immunity are fitness-related traits that trade-off with each other. Parasite-mediated theories of sexual selection suggest, however, that higher-quality males should suffer smaller costs to reproduction-related traits and behaviours (e.g., sexual display) from an immune challenge because these males possess more resources with which to deal with the challenge. We used Gryllus texensis field crickets to test the prediction that attractive males should better maintain the performance of fitness-related traits (e.g., calling effort) in the face of an immune challenge compared with unattractive males. We found no support for our original predictions. However, that immune activation causes attractive males to significantly increase their calling effort compared with unattractive males suggests that these males might terminally invest in order to compensate for decreased future reproduction.

Sex differences in the effects of juvenile and adult diet on age-dependent reproductive effort.

Sexual selection should cause sex differences in patterns of resource allocation. When current and future reproductive effort trade off, variation in resource acquisition might further cause sex differences in age-dependent investment, or in sensitivity to changes in resource availability over time. However, the nature and prevalence of sex differences in age-dependent investment remain unclear. We manipulated resource acquisition at juvenile and adult stages in decorated crickets, Gryllodes sigillatus, and assessed effects on sex-specific allocation to age-dependent reproductive effort (calling in males, fecundity in females) and longevity. We predicted that the resource and time demands of egg production would result in relatively consistent female strategies across treatments, whereas male investment should depend sharply on diet. Contrary to expectations, female age-dependent reproductive effort diverged substantially across treatments, with resource-limited females showing much lower and later investment in reproduction; the highest fecundity was associated with intermediate lifespans. In contrast, long-lived males always signalled more than short-lived males, and male age-dependent reproductive effort did not depend on diet. We found consistently positive covariance between male reproductive effort and lifespan, whereas diet altered this covariance in females, revealing sex differences in the benefits of allocation to longevity. Our results support sex-specific selection on allocation patterns, but also suggest a simpler alternative: males may use social feedback to make allocation decisions and preferentially store resources as energetic reserves in its absence. Increased calling effort with age therefore could be caused by gradual resource accumulation, heightened mortality risk over time, and a lack of feedback from available mates.

Energetic cost of vibrational signalling in a leafhopper

Communication via substrate-borne vibrations is the most widespread form of acoustic communication in arthropods. However, remarkably little is known about physiological sources of selection on vibrational communication systems, in particular those underlying mate choice and male competition. Here, we studied the energetic cost of vibrational signalling in the leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae). We measured O2 consumption of a single male for 15–30 min using the closed-bottle method and a lifetime-based optode, while we recorded emitted vibrational signals with a laser vibrometer. Males were emitting three types of vibrational signals (advertisement calls, masking signals and pulse signals), and the respiration rate was significantly positively correlated with the cumulative signalling time. Our results showed that vibrational signalling was around 12.4 times energetically more demanding than resting. Furthermore, production of masking signals emitted in rivalry situations was as energetically demanding as production of advertisement calls used in sexual communication between partners. We also assessed the effect of calling effort on male survival. We determined calling effort by playback experiments once every week of male’s adult life until death. The average male longevity was 50 days, and survival was negatively correlated with the number of emitted advertisement calls, calling rate and calling time in early life. Considering that in mating systems based on vibrational signals, communication occurs in a changing social environment, more detailed studies on indirect costs of signalling in such systems may provide new insights into mechanisms that lead to adaptive plasticity in male sexual behaviour.

Prior mating success can affect allocation towards future sexual signaling in crickets.

Fitness is often correlated with the expression level of a sexually selected trait. However, sexually selected traits are costly to express such that investment in their expression should be optimised to maximize their overall fitness gains. Social interactions, in the form of successful and unsuccessful matings, may offer males one type of feedback allowing them to gauge how to allocate their resources towards sexual signaling. Here we tested whether adult male black field crickets (Teleogryllus commodus) modify the extent of their calling effort (the sexually selected trait) in response to successful and unsuccessful matings with females. To examine the effect that mating interactions with females have on investment into sexual signaling, we monitored male calling effort after maturation and then provided males with a female at two points within their life, manipulating whether or not males were able to successfully mate each time. Our results demonstrate that males alter their investment towards sexual signaling in response to successful matings, but only if the experience occurs early in their life. Males that mated early decreased their calling effort sooner than males that were denied a mating. Our results demonstrate that social feedback in the form of successful and unsuccessful matings has the potential to alter the effort a male places towards sexual signaling.

Condition dependence of female choosiness in a field cricket.

Females generally choose mates that produce the loudest, brightest or most elaborate sexual displays, and these costly male displays are predicted to be condition dependent. However, mate choice itself is a costly behaviour also expected to be condition dependent. Male fall field crickets, Gryllus pennsylvanicus, produce a conspicuous long-distance calling song that attracts females and is condition dependent. In this study, we tested the condition dependence of female preferences (preference function and choosiness) for male calling effort in G.pennsylvanicus. We manipulated female condition by raising crickets from hatching on either a low- or high-quality diet. In a series of two-speaker phonotaxis trials, both low- and high-condition females preferred playbacks reflecting greater calling effort. However, relative to low-condition females, high-condition females took significantly longer to make a choice, were more likely to fail to choose within the time allotted for a phonotaxis trial and significantly increased their latency to choose over the course of multiple trials. We discuss these results with respect to the possibility that female G.pennsylvanicus may be foraging for direct benefits when they choose their mates.