Early learning of discrete call variants in red crossbills: implications for reliable signaling

The identification of appropriate companions and mates is essential to both speciation and the maintenance of species through prezygotic isolation. In many birds, social assortment is mediated by vocalizations learned through imitation. When imitative vocal learning occurs throughout life, emergent shared signals reflect current social associations. However, when vocal and genetic variation arises among populations, shared learned signal variants have a potential to reflect cultural or genetic origin and to limit social and reproductive intermixing, provided that signal learning occurs prior to dispersal. The red crossbill (Loxia curvirostra) is a bird species in which discrete contact call variants are associated with morphological variation, raising the possibility that learned calls play a role in limiting intermixing. I examined the process of early call learning to determine if contact call variants have a potential to limit intermixing in crossbills. I conducted a captive playback study to nestlings to evaluate potential learning predispositions. I also cross-fostered nestlings to adoptive adult pairs of either their own or a different call variant than their biological parents to assess the degree of vocal learning plasticity. Results show that young crossbills imitate the call structures of adoptive parents, generating shared family-specific calls, which could facilitate family cohesion. Learning processes that generate family-specific calls could also ensure that discrete call variants are transmitted across generations, making call variants reliable signals of crossbills’ morphological and genetic backgrounds.     

Territorial vocal behavior in hybrid smooth froglets, Geocrinia laevis complex (Anura: Myobatrachidae)

Males of the parapatically distributed myobatrachid frogs Geocrinia laevis and G. victoriana have highly divergent advertisement calls. Furthermore, the two species differ strongly in the complexity of their vocal repertoires, with males of G. victoriana possessing, and those of G. laevis lacking, a distinct territorial vocalization (encounter call). We investigated the territorial vocal behavior of males in a persistent natural hybrid population. Most hybrid males possessed encounter calls functionally equivalent to those of G. victoriana, that were produced following exposure to playback of recorded advertisement calls presented at >110 dB peak sound pressure level. The territorial acoustic responses were not associated with an index of hybridity derived from the structure of the advertisement call, suggesting genetic and functional decoupling of the two components of the vocal repertoire; i.e., advertisement calls and encounter calls. This decoupling may be the result of sexual selection favouring those hybrids with pronounced territorial behavior and the associated vocalization, regardless of the structure of their advertisement calls.Communicated by A. Mathis     

Species-specificity and individual variation in the song of male Nathusius’ pipistrelles (<Emphasis Type="Italic">Pipistrellus nathusii</Emphasis>)

Sequences of the advertisement calls produced by male Nathusius’ pipistrelles (Pipistrellus nathusii) during the autumn mating period were recorded from individuals at two separate sites in Antrim, Northern Ireland, in August 2004. Several male roosts were found at these sites in close proximity to a single maternity roost, each containing approximately 200 adult females and their young. Analysis of measured parameters of four identified call types revealed that there were significant differences in call structure between sites and between individuals. Playback experiments, performed outside the adult female and juvenile roost sites, comprised of experimental advertisement call sequences of P. nathusii, Pipistrellus pygmaeus and Pipistrellus pipistrellus and control sound recorded without bats present (silence). Response was measured by simultaneously recording ultrasound during playbacks and counting the number of echolocation pulses identified as those of P. nathusii above a predetermined amplitude threshold. Significantly greater numbers of P. nathusii echolocation pulses were recorded during playback of male P. nathusii advertisement calls than during playback of congeners’ advertisement calls and control sound. The number of echolocation pulses recorded was similar during playback of P. pipistrellus and P. pygmaeus advertisement calls and silence. We suggest that, due to call complexity, male P. nathusii advertisement calls should be classified as ‘song’. Species-specificity and individual variation suggests that the songs of male P. nathusii have the potential to play a role in mate attraction and mate assessment.     

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.     

The alarm call system of wild black-fronted titi monkeys, <Emphasis Type="Italic">Callicebus nigrifrons</Emphasis>

Upon encountering predators, many animals produce specific vocalisations that alert others and sometimes dissuade the predators from hunting. Callicebus monkeys are known for their large vocal repertoire, but little is known about the function and meaning of most call types. We recorded a large number of natural predator responses from five different groups of black-fronted titi monkeys in their Atlantic forest habitat in South Eastern Brazil. When detecting predatory threats, adult group members responded with call sequences that initially consisted of two brief, high-pitched calls with distinct frequency contours. Call A was mainly given to raptors but also to predatory capuchin monkeys and other threats within the canopy, while call B was given to predatory or non-predatory disturbances on the ground. In later parts of the sequences, we also recorded a high-pitched unmodulated call C and various low-pitched loud calls. Results therefore suggest that calls A and B provide listeners with rapid and reliable information about the general classes of danger experienced by the caller, while obtaining more specific information through other call types and combinations and behavioural responses. We discuss these findings in relation to current evolutionary theory of primate communication.     

Chick-a-dee call syntax,social context,and season affect vocal responses of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls in many chickadee (Poecile) species are common vocal signals used in a diversity of social contacts. The calls consist of four notes, A, B, C, and D, which follow simple rules of syntax (note ordering and composition) to generate many unique call types. We used field playbacks with Carolina chickadees, P. carolinensis, to ask whether violations of a syntactical rule affected their vocal responses. We show that chickadee responses to typical calls (e.g. AAAACCCC and CCCCDDDD) differ from responses to atypical calls (e.g. CACACACA and DCDCDCDC) depending on playback note composition, season, and social context (presence of heterospecifics). In the fall/winter, playbacks of typical calls with A and C notes elicited the greatest number of A and B notes in chick-a-dee call responses and typical calls with D notes elicited the greatest number of C notes, when in the presence of heterospecifics. In contrast, the corresponding atypical calls did not elicit similar responses. This suggests communicative significance is lost in calls that violate a rule of syntax in the fall/winter. In the spring, neither chickadee feebeefeebay song rate nor chick-a-dee calls responses differed by playback type. We suggest that call syntax is less salient for mated pairs in the spring than it is for fall/winter flocks that rely more on conspecific communication for foraging success and flock cohesion. This study represents the first experimental evidence that chickadees attend to both note composition and ordering in chick-a-dee calls.Communicated by W.A. Searcy     

The role of synchronized calling,ambient light,and ambient noise,in anti-bat-predator behavior of a treefrog

Summary Male treefrogs, Smilisca sila (Hylidae), produce calls of varying complexity and demonstrate a remarkable ability to synchronize their calls with those of neighbors. The bat Trachops cirrhosus eats frogs and uses the frogs' advertisement calls as locational cues. The bats are less likely to respond to synchronous calls than to asynchronous calls, and when given a choice prefer complex calls to simple calls.Experiments with bat models indicate that, like other frogs, S. sila probably uses visual cues to detect hunting bats. In response to bat models the frogs decreased both the number and the complexity of their calls. The calling behavior of the frogs was sampled in the field during periods with and without artificial illumination. The frogs produced fewer and less complex calls, and they tended to call from more concealed sites, during the period without illumination, when presumably it would have been more difficult for the frogs to detect hunting bats. S. sila tended to call from sites with higher ambient noise level, the noise primarily originating from waterfalls. The frequencies of the dominant energies in the waterfall sounds completely overlapped the frequency range of the S. sila call; thus waterfalls might mask the frog calls. When given a choice between calls produced near and away from waterfall sounds, bats preferred the latter.     

Predation affects alarm call usage in female Diana monkeys (Cercopithecus diana diana)

Diana monkeys produce acoustically distinct calls to a number of external events, including different types of predators. In a previous study, we found population-wide differences in male alarm call production in Taï Forest, Ivory Coast, and on Tiwai Island, Sierra Leone, mostly likely originating from differences in predator experience. In Taï Forest, leopards (Panthera pardus) are common but on Tiwai Island they have been absent for decades, while the predation pressure from crowned eagles (Stephanoaetus coronatus) has been similar. To further evaluate the impact of predator experience, we here analyse the vocal behaviour of female Diana monkeys in both habitats. Female Diana monkeys produce predator-specific alarm calls, alert calls and contact calls in response to predators, suggesting that their calls serve in a broader range of functions compared to males. Results showed that females produced the same call types at both sites, despite the differences in predator fauna. Regarding call usage, leopard alarm calls were extremely rare on Tiwai Island, but not in Taï Forest, whereas we found no differences in eagle alarm call production. When comparing response latencies, Tiwai females were slower to respond to both predators compared to Taï females. Finally, we found no habitat-specific acoustic differences in the alert and predator-specific alarm calls, but significant differences in frequency-based parameters of contact calls. Overall, our results suggest that ontogenetic experience can affect primate vocal behaviour in both usage and acoustic structure but that the way in which particular call types are affected may be closely linked to function.     

No reproductive character displacement in male advertisement signals of Hyla japonica in relation to the sympatric H. suweonensis

Reproductive interaction between closely related taxa may leave a distinctive signature in which populations of interacting taxa are more dissimilar in sympatry than in allopatry. An ideal condition for such a pattern of reproductive character displacement (RCD) may occur when a population has limited gene flow and experiences strong selection pressure, exerted by an interacting taxon in areas of sympatry. In Korea, there are two closely related treefrog species: Hyla japonica, which is distributed widely throughout the country, and Hyla suweonensis, which occurs sympatrically in a narrow strip of western coastal plains. H. suweonensis is only found within the distribution of H. japonica. These two species have a similar single-note call structure. Here, we tested the possibility of RCD in H. japonica by examining geographic variation in advertisement calls. Although means of temporal and spectral characters were significantly different between the two species, sympatric populations of H. japonica and H. suweonensis overlapped in distributions of most characters. Furthermore, allopatric and sympatric H. japonica populations did not differ in all call characters. Weak genetic differentiation between sympatric and allopatric populations of H. japonica implied either substantial gene flow or recent genetic isolation. Possible explanations for no RCD in male advertisement calls of H. japonica include a difference in fine temporal characteristics between the two species, migration between sympatric and allopatric localities in H. japonica, RCD in female preferences in H. japonica, and weak selection pressure by H. suweonensis.     

Vocal competition in male Xenopus laevis frogs

Male Xenopus laevis frogs produce underwater advertisement calls that attract gravid females and suppress calling by male competitors. Here we explore whether groups of males establish vocal ranks and whether auditory cues alone suffice for vocal suppression. Tests of male–male pairs within assigned groups reveal linear vocal dominance relations, in which each male has a defined rank. Both the duration over which males interact, as well as the number of competitive opportunities, affect linearity. Linear dominance across the group is stable for about 2 weeks; rank is dynamic. Males engage in physical interactions (clasping) while paired but clasping and vocal rank are not correlated. Playbacks of advertisement calls suppress calling and calls from high- and low-ranking males are equally effective. Thus, auditory cues alone suffice to suppress vocal behavior. Playback intensities equivalent to a nearby male advertising effectively suppress calling while low-intensity playbacks are either ineffective or stimulate vocal behavior. X. laevis advertisement calls are biphasic, composed of alternating fast and slow click trills. Approximately half the males tested are more vocally suppressed by all slow than by all fast trills; thus, these males can distinguish between the two phases. The fully aquatic family Pipidae diverged from terrestrial ancestors approximately 170 mya. Vocal suppression in the X. laevis mating system may represent the translation of an ancient anuran social strategy to underwater life.     

Population frequencies of alternative male phenotypes in tree lizards: geographic variation and common-garden rearing studies

Tree lizards (Urosaurus ornatus) vary in throat fan (dewlap) color. Earlier, we described five dewlap types (Orange, Orange-Blue, Yellow, Yellow-Blue, and Blue), and reported that only males had blue in the dewlap and that presence or absence of a discrete blue patch was correlated with male alternative reproductive phenotypes in a central Arizona population. Here, with a modified scheme characterizing two dewlap elements, background color (orange, yellow, blue) and blue patch occurrence, we assessed: (1) sexual, annual, and geographic variation in the frequencies of dewlap elements; (2) simple habitat correlates; and (3) the effects of laboratory rearing regime on dewlap type. Within a population, frequencies of males and females expressing orange or yellow backgrounds did not differ, suggesting that control of background is similar in the sexes. Within several populations, frequencies of the dewlap elements did not differ across years (and probably generations), indicating that phenotype frequencies are relatively stable. Among five populations frequencies of background colors varied, as did frequencies of male types (blue patch present or absent). Dewlap frequencies did not correlate with habitat (boulders or mesquite trees), although few populations were sampled. In male and female offspring reared from eggs to sexual maturity in a common-garden laboratory study, background color frequencies in both sexes and blue patch frequencies in males differed among offspring from different populations. Offspring frequencies matched respective parental population frequencies. Results suggest that among-population variation in frequencies of the two dewlap elements are mediated by differences in genetics, in maternal effects, or both. Thus, differences in male behavior functionally linked to the blue patch also may be controlled by genetic or maternal effects. Received: 17 January 1997 / Accepted after revision: 30 August 1997     

Co-infection patterns and geographic distribution of a complex pathosystem targeted by pathogen-resistant plants

Increasingly, pathogen-resistant (PR) plants are being developed to reduce the agricultural impacts of disease. However PR plants also have the potential to result in increased invasiveness of nontarget host populations and so pose a potential threat to nontarget ecosystems. In this paper we use a new framework to investigate geographical variation in the potential risk associated with unintended release of genetically modified alfalfa mosaic virus (AMV)-resistant Trifolium repens (white clover) into nontarget host populations containing AMV, clover yellow vein virus (ClYVV), and white clover mosaic virus (WCIMV) in southeastern Australia. Surveys of 213 sites in 37 habitat types over a 300 000-km2 study region showed that T. repens is a significant weed of many high-conservation-value habitats in southeastern Australia and that AMV, ClYVV, and WClMV occur in 15-97% of nontarget host populations. However, T. repens abundance varied with site disturbance, habitat conservation value, and proximity to cropping, and all viral pathogens had distinct geographic distributions and infection patterns. Virus species frequently co-infected host plants and displayed nonindependent distributions within host populations, although co-infection patterns varied across the study region. Our results clearly illustrate the complexity of conducting environmental risk assessments that involve geographically widespread, invasive pasture species and demonstrate the general need for targeted, habitat- and pathosystem-specific studies prior to the process of tiered risk assessment.     

Limited geographic variation in the acoustic structure of and responses to adult male alarm barks of African green monkeys

The global diversity of human languages is a remarkable feature of our species, which requires a capacity for rapid vocal learning. Given that primate alarm calling systems have played an important role in the language origin debate, identifying geographic variation in primate alarm calls and understanding the underlying causal mechanisms are important steps to help uncover evolutionary precursors to language. This study investigates geographic variation in the alarm bark of the widely distributed African green monkey (Chlorocebus). To quantify geographic variation in spectral and temporal call structure, acoustic analysis was used to compare the adult male barks of green monkeys (Chlorocebus sabaeus) and two subspecies of vervet (Chlorocebus pygerythrus pygerythrus and Chlorocebus pygerythrus hilgerti). Playback experiments were also carried out to test whether adult male vervets would distinguish between the barks of own-group males, unknown conspecific males and green monkey males. Acoustic analysis showed that, whilst similar in overall structure, the barks of green monkeys could be distinguished from vervet barks with a high degree of accuracy; the barks of vervet subspecies could also be discriminated, although to a lesser degree. Males responded most strongly to unknown conspecific males’ barks, and exhibited responses typical of leopard-avoidance and territorial defence. Taken together, these findings indicate that variation in alarm calls can be best explained by phylogenetic distance, and that intra- and inter-species differences are relevant during social interactions. Moreover, barks may function as an alarm and display call, which could explain the observed sexual dimorphism in barks in this genus.     

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.     

The function of call alternation in the African reed frog (Hyperolius marmoratus): precise call timing prevents auditory masking

The function of call alternation in the African painted reed frog, Hyperolius marmoratus was studied. Males actively avoided call overlap with neighboring males in their natural habitat. Advertisement calls produced by groups of two or three males showed less overlap than expected if they called at random. In addition, isolated males significantly reduced their calling rate to match the periodicity of a playback of periodic tone pulses, with vocalizations given during the silent intervals between tones. Gap-detection experiments showed that males suppressed vocalizations during playbacks of constant-frequency tone bursts and gave more calls during silent periods than expected by chance. Females discriminated against conspecific advertisement calls with many pulses in favor of calls with few or no pulses. This suggests that there would be little selection pressure on males to alternate calls so that pulses are not obscured. To test if call alternation functions to make calls more conspicuous, females were presented with identical conspecific advertisement calls from two speakers in four different temporal patterns: simultaneous, overlapping, abutting, and alternating. Females did not discriminate when calls were presented in a simultaneous, abutting, or alternating time pattern. When calls overlapped with the trailing call delayed from 0.5 to 70 ms females discriminated in favor of the leading call. When the intensity of the leading call was reduced by 6 dB the preference for the leading call was maintained when calls overlapped by 2 and 40 ms but was abolished or reversed at 0.5 and 70 ms, respectively. These results support the notion that the second of two partially overlapping calls was acoustically masked, rendering female painted reed frogs unwilling to approach or unable to locate such calls. It is suggested that either simultaneous masking or the precedence effect are responsible for the observed behavior. Acoustic masking of the second call by the first when calls overlapped was maintained even when the frequency of the first call was altered by 150 Hz above and below the more preferred frequency of the second call. Received: 13 April 1995/Accepted after revision: 5 November 1995     

A spatial gradient in the potential reproductive output of the sea mussel <Emphasis Type="Italic">Mytilus californianus</Emphasis>

Spatial variation in reproductive output from different populations within a region could have important consequences for recruitment, and cascading effects on populations and communities of marine species, but is rarely examined over meso-scales (i.e., tens to hundreds of kilometers). In this study, reproduction in the dominant mid-intertidal mussel, Mytilus californianus, was examined from sites spanning Point Conception, California over a 6-month period (March–August 2000). There was a dramatic geographic pattern in the relationship between size and potential reproductive output that was qualitatively similar across all 6 months sampled. Increases in allocation to reproductive tissue with increasing body size occurred at all sites, but the slope nearly doubled at sites south of Point Conception compared to northern sites. The spatial variation in size-specific reproductive output, coupled with additional spatial gradients in mussel density and size distributions, combined to increase total reproductive output by over eightfold at southern relative to northern sites. This study highlights the need to explicitly examine spatial patterns of reproductive output at these meso-scales, in order to better understand connectivity and source–sink dynamics in marine systems.     

Aggressive thresholds in Dendropsophus ebraccatus: habituation and sensitization to different call types

Males in many chorusing anuran species use aggressive calls during defense of calling spaces from other males. The minimal intensity of another male’s vocalizations that elicits an aggressive call response has been termed the aggressive threshold. Previous studies of aggressive thresholds have shown that they are plastic: males habituated (increased their aggressive thresholds) in response to repeated presentation of stimuli above initial threshold levels. Habituation likely contributes to the stable chorus structure of these species, in which aggressive calling is rare compared to advertisement calls. I have observed high levels of aggressive calling in the treefrog Dendropsophus ebraccatus, suggesting that males of this species do not habituate. In this study, I investigated the plasticity of aggressive thresholds in D. ebraccatus. I measured the aggressive thresholds of males before and after suprathreshold stimulation by both advertisement and aggressive calls. I found that the different call types had different effects: males habituated to advertisement calls but lowered their aggressive thresholds in response to aggressive calls. I consider the latter response to be an example of sensitization, a behavior that has been documented infrequently in vocalizing anurans. Sensitization is a plausible mechanism responsible for the high levels of aggressive calling observed in this species. Given the high costs of aggressive calling, however, it is unclear why a mechanism that increases aggressive call output would be maintained.     

Acoustically mediated neighbor recognition in the North American bullfrog,Rana catesbeiana

Summary Playback experiments were conducted to determine whether territorial male bullfrogs (Rana catesbeiana) were capable of discriminating between advertisement calls of neighbors and strangers. Territorial males adjacent to subject males were removed and replaced with a speaker which broadcast calls of a stranger or the removed male. Ten of 11 males responded more strongly to calls of strangers than to calls of neighbors. When advertisement calls of neighbors were broadcast to subject males from positions within the removed neighbor's territory and from positions opposite the subject male, all 9 males tested responded more strongly to calls of a neighbor broadcast from a new position than to playbacks of the same call broadcast within the removed neighbor's territory. Because male bullfrogs recognize familiar calls and associate these calls with a particular direction or location, these data provide the first evidence for acoustically mediated neighbor recognition in frogs.     

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.