Aggressive Calls Research Articles

Correction to: Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog Dendropsophus ebraccatus

Correction to: Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog Dendropsophus ebraccatus

AGGRESSIVE BEHAVIOR OF Rheohyla miotympanum (ANURA: HYLIDAE) IN NORTHERN HIDALGO, MEXICO

Anurans communicate primarily through calls, which can be classified into three categories (reproductive, defensive and aggressive) according to the social context in which they occur. Aggressive calls are usually emitted by males to defend habitat resources (calling sites, females), generally accompanied by physical aggression. Here, we report aggressive behavior between two Rheohyla miotympanum males, possibly triggered by defense of the calling site and for the opportunity for amplexus (receptive female, approximately 80 cm from the scene). This behavior was characterized by physical contact (fight) and the emission of aggressive calls between both males. Future studies are required that make specific observations of the calls, considering the proximity and density of conspecifics, which could help to understanding the main causes of the aggressive behavior of this and other anuran species.

SEXUAL DIFFERENTIATION OF AGGRESSIVE BEHAVIOR IN THE CHICKS OF THE BLACK-HEADED GULL (<i>LARUS RIDIBUNDUS</i>, LARIDAE, CHARADRIIFORMES) IN THE NATURAL ENVIRONMENT

Sexual differentiation of social behavior in gulls and its mechanisms remain unexplored beyond the breeding season. We described the development of aggressive territorial behavior in males and females of black-headed gulls at the age of 1–4 weeks, modeling the intrusion of a peer to the nesting territory. We also hypothesized that the sex differentiation of aggressive behavior may appear as a consequence of the development of small early differences between siblings in behavioral stress response. To test this assumption, we investigated the relationship between the priority among brood in aggressive contact with the intruder, and the within-broods level of activity of a chick to stress. To measure the behavioral stress response, we used the social isolation of chicks within a small water area with an island in the middle. Longer attempts to swim outside the fenced area were regarded as a more proactive stress response. At the age of up to 3 weeks, there were no sex differences in the aggressiveness, but the stress response of males was more proactive than that of their sisters, and a more proactive chick in the brood was usually the first to attack the intruder. At the fourth week of life, the aggressiveness of males increased significantly, and in broods of two sexes, brothers began to play a leading role in protecting the nesting territory in the absence of parents. They attacked the intruder more often and made aggressive calls more frequently. Thus, we were the first to reveal sexual differentiation of territorial behavior in gull chicks in the pre-fledging period. Our results suggest that under natural conditions, where the intruder does not persist in staying in the other nest, but recedes immediately when counteracted, more proactive males use to attack the intruder earlier than sisters do. As a result, they gain experience of aggressive interactions, and develop higher abilities of aggressive responses to social challenges.

Acoustic plasticity in Boana goiana (Lutz, 1968) (Anura, Hylidae): how males respond to successive interactions with conspecific competitors

ABSTRACT During the breeding season, hundreds of anurans agglomerate at spawning sites, where a diversity of social contexts arise. In this scenario, anurans may alter their vocal repertoire according to the immediate social context, to overcome intraspecific competition. To evaluate the acoustic response of Boana goiana to successive interactions with a conspecific competitor, the present study was based on comparing the repetition rates of advertisement and aggressive calls of B. goiana focal males exposure to repeated artificial advertisement calls in 10 playback sessions. We observed that B. goiana males altered their acoustic behaviour in response to the simulated arrival of a new competitor. Males emitted less advertisement calls and more aggressive calls with the arrival of the competitors. Temperature and body condition were not important predictors of continuity of males in the experiment or the call repetition rates in the pre-playback session. However, the body condition influenced the total delta advertisement calls (differences in the call rate emission between end and the beginning of the experiment), indicating that higher values of body conditions allow males to show smaller reductions in the emission of advertisement calls over time in the presence of a competitor.

Auditory processing for action selection in bats

Bats are auditory specialists, processing acoustic signals to guide their behaviors, including prey tracking, navigation and communication. In this talk I will provide an overview of my work related to how bats analyze and process signals for action-selection; specifically prey tracking and background clutter segregation—work inspired by research from Jim Simmons’s lab. I will also give an overview of the line of research of my current lab, neural mechanisms for auditory processing of communication signals. There is strong evidence that context plays a role in the processing of acoustic signals. Yet, the mechanisms that govern this process are still not fully understood. Eptesicus fuscus bats emit a wide array of communication calls, including food claiming calls, aggressive calls and appeasement calls. We developed a novel competitive foraging task to explore the role of behavioral context in auditory responses to social calls. With this approach, we recorded neural population responses from the IC of freely interacting bats. Analysis of our neural recordings from the IC show stronger population responses to individual calls during behaviorally aggressive events. These results indicate that behavioral context plays a role in the modulation of neuronal population responses to social vocalizations in the bat IC.

Effects of Different-Syllable Aggressive Calls on Food Intake and Gene Expression in Vespertilio sinensis.

Social animals enjoy colony benefits but are also exposed to social stress, which affects their physiology in many ways, including alterations to their energy intake, metabolism, and even gene expression. Aggressive calls are defined as calls emitted during aggressive conflicts between individuals of the same species over resources, such as territory, food, or mates. Aggressive calls produced by animals in different aggressive states indicate different levels of competitive intentions. However, whether aggressive calls produced in different aggressive states exert different physiological effects on animals has yet to be determined. Importantly, bats live in clusters and frequently produce aggressive calls of different syllables, thus providing an ideal model for investigating this question. Here, we conducted playback experiments to investigate the effects of two types of aggressive calls representing different competitive intentions on food intake, body mass, corticosterone (CORT) concentration, and gene expression in Vespertilio sinensis. We found that the playback of both aggressive calls resulted in a significant decrease in food intake and body mass, and bats in the tonal-syllable aggressive-calls (tonal calls) playback group exhibited a more significant decrease when compared to the noisy-syllable aggressive-calls (noisy calls) playback group. Surprisingly, the weight and food intake in the white-noise group decreased the most when compared to before playback. Transcriptome results showed that, when compared to the control and white-noise groups, differentially expressed genes (DEGs) involved in energy and metabolism were detected in the noisy-calls playback group, and DEGs involved in immunity and disease were detected in the tonal-calls playback group. These results suggested that the playback of the two types of aggressive calls differentially affected body mass, food intake, and gene expression in bats. Notably, bat responses to external-noise playback (synthetic white noise) were more pronounced than the playback of the two aggressive calls, suggesting that bats have somewhat adapted to internal aggressive calls. Comparative transcriptome analysis suggested that the playback of the two syllabic aggressive calls disrupted the immune system and increased the risk of disease in bats. This study provides new insight into how animals differ in response to different social stressors and anthropogenic noise.

Network analysis reveals context-dependent structural complexity of social calls in serrate-legged small treefrogs.

Vocal communication plays an important role in survival, reproduction, and animal social association. Birds and mammals produce complex vocal sequence to convey context-dependent information. Vocalizations are conspicuous features of the behavior of most anuran species (frogs and toads), and males usually alter their calling strategies according to ecological context to improve the attractiveness/competitiveness. However, very few studies have focused on the variation of vocal sequence in anurans. In the present study, we used both conventional method and network analysis to investigate the context-dependent vocal repertoire, vocal sequence, and call network structure in serrate-legged small treefrogs Kurixalus odontotarsus. We found that male K. odontotarsus modified their vocal sequence by switching to different call types and increasing repertoire size in the presence of a competitive rival. Specifically, compared with before and after the playback of advertisement calls, males emitted fewer advertisement calls, but more aggressive calls, encounter calls, and compound calls during the playback period. Network analysis revealed that the mean degree, mean closeness, and mean betweenness of the call networks significantly decreased during the playback period, which resulted in lower connectivity. In addition, the increased proportion of one-way motifs and average path length also indicated that the connectivity of the call network decreased in competitive context. However, the vocal sequence of K. odontotarsus did not display a clear small-world network structure, regardless of context. Our study presents a paradigm to apply network analysis to vocal sequence in anurans and has important implications for understanding the evolution and function of sequence patterns.

Vocal repertoire and acoustic variation in a treefrog (Boana ericae) (Amphibia, Anura, Hylidae) endemic to the Chapada dos Veadeiros, Central Brazil

ABSTRACT Despite the great diversity of Brazilian anuran species, there are still many knowledge gaps about the acoustic communication of these animals. Among the species, those classified as ‘Data Deficient’ have the greatest gaps in knowledge on their behavior. This is the case of Boana ericae, a species belonging to the Boana pulchella group, endemic to the Chapada dos Veadeiros National Park region, in the northeast of the state of Goiás, Central Brazil. Three distinct call types (A, B, and C) are currently known for B. ericae, with the type A call associated with attracting reproductive partners and the type C call presenting a territorial function. We recorded the vocalizations of 10 individuals of this species and found the presence of vocalizations composing three new note types (D, E, and F). Our results indicate that air temperature and body condition influenced the acoustic parameters of the advertisement and aggressive calls of this species. We also observed that some acoustic parameters of the advertisement calls can be used for individual recognition for showing greater variation among individuals than intra-individually. Our results add new information regarding the vocal repertoire in this species, expanding their known intra-individual classification of the acoustic parameters.

Filling the knowledge gaps of Paratelmatobius mantiqueira (Anura: Leptodactylidae): tadpole, acoustic repertoire, and life history traits

ABSTRACT We monitored a recently discovered population of Paratelmatobius mantiqueira for 13 months and gathered new data for the species: external morphology of tadpoles, acoustic repertoire, and life history traits. We also collected unprecedented data on behaviours and interactions of adults and tadpoles observed during monitoring. Based on natural markings of P. mantiqueira adults, we estimated the effective population size and estimated their home range. With circular statistics, we tested whether they were seasonally active and evaluated how humidity and temperature influenced the detectability of the species. We found that tadpoles and advertisement calls of P. mantiqueira differed from congeneric species. We also described the release and aggressive calls. We found that the species has a small home range, with probable resident females. Temperature and humidity positively influenced the detectability of P. mantiqueira; encounters varied seasonally. Paratelmatobius mantiqueira is a strictly forest species, found mainly in leaf litter and associated with muddy areas in rocky outcrops of highland forests. Our study provides new data about P. mantiqueira, which may help future integrative taxonomy approaches and contribute to the conservation of this species.

Sensory biases in response to novel complex acoustic signals in male and female grey treefrogs, Hyla chrysoscelis.

The sensory bias hypothesis proposes that female preferences for male sexual signalling traits evolved in contexts other than mating. Individuals of both sexes may experience similar selection pressures in these contexts; thus males may have similar biases to females for variation in signal traits. We tested this prediction in the grey treefrog, Hyla chrysoscelis, in which males produce simple advertisement calls, but females are more attracted to certain novel complex stimuli. We recorded males' responses to playbacks of both simple advertisement calls and complex calls consisting of the advertisement call with an acoustic appendage (filtered noise, or heterospecific call pulses) either leading or following the call. We tested females' preferences for the same stimuli in phonotaxis tests. We found evidence for a sensory bias in both sexes: males gave more aggressive calls in response to complex stimuli and females sometimes preferred complex over simple calls. These biases were not universal and depended on both temporal order and appendage characteristics, but how these effects manifested differed between the sexes. Ultimately, our approach of studying biases of both sexes in response to novel mating signals will shed light on the origin of mating preferences, and the mechanisms by which sensory biases operate.

Positive-to-negative behavioural responses suggest hedonic evaluation in treefrog mate choice.

Sexual competition hinges on the ability to impress other conspecifics, to drive them away or attract them. In such cases, the selective environment may be hedonic or affective in nature, as it consists of the evaluations of the individuals making the decisions. This may contribute to the power of sexual selection because evaluations may range from positive to negative rather than simply from positive to neutral. Selection due to mate choice may therefore be stronger than currently appreciated. Further, change in preferred mate types can occur simply by changes (flips) in the evaluation of similar display features, adding to the dynamism of sexual selection as well as its strength. We tested the hypothesis of positive-to-negative behavioural responses in mate choice with a playback experiment using two treefrog species with 'mirror image' structures in their advertisement and aggressive calls. Female treefrog responses ranged from approach to evasion, and the presence of an aversive stimulus tainted evaluation of an attractive stimulus. Further, females in the two species showed flips in approach/evasion of stimuli with comparable signal structure. These results suggest that hedonic evaluation may have an important role in mate choice and showcase how mechanistic analysis can help understand evolutionary processes.

Function of a multimodal signal: A multiple hypothesis test using a robot frog.

Multimodal communication may evolve because different signals may convey information about the signaller (content-based selection), increase efficacy of signal processing or transmission through the environment (efficacy-based selection), or modify the production of a signal or the receiver's response to it (inter-signal interaction selection). To understand the function of a multimodal signal (aggressive calls+toe flags) emitted by males of the frog Crossodactylus schmidti during territorial contests, we tested two hypotheses related to content-based selection (quality and redundant signal), one related to efficacy-based selection (efficacy backup), and one related to inter-signal interaction selection (context). For each hypothesis we derived unique predictions based on the biology of the study species. In a natural setting, we exposed resident males to a robot frog simulating aggressive calls (acoustic stimulus) and toe flags (visual stimulus), combined and in isolation, and measured quality-related traits from males and local levels of background noise and light intensity. Our results provide support to the context hypothesis, as toe flags (the context signal) are insufficient to elicit a receiver's response on their own. However, when toe flags are emitted together with aggressive calls, they evoke in the receiver qualitatively and quantitatively different responses from that evoked by aggressive calls alone. In contrast, we found no evidence that toe flags and aggressive calls provide complementary or redundant information about male quality, which are key predictions of the quality and redundant signal hypotheses respectively. Finally, the multimodal signal did not increase the receiver's response across natural gradients of light and background noise, a key prediction of the efficacy backup hypothesis. Toe flags accompanying aggressive calls seem to provide contextual information that modify the receiver's response in territorial contests. We suggest this contextual information is increased motivation to escalate the contest, and discuss the benefits to the signallers and receivers of adding a contextual signal to the aggressive display. Examples of context-dependent multimodal signals are rare in the literature, probably because most studies focus on single hypotheses assuming content- or efficacy-based selection. Our study highlights the importance of considering multiple selective pressures when testing multimodal signal function.

The Vocal Repertoire of the Bearded Capuchin (Cebidae: Sapajus libidinosus): Implications for Understanding the Complexity of Neotropical Primate Communication

Vocal communication is an essential aspect of primate social behaviour. The bearded capuchin Sapajus libidinosus is endemic to Brazil, and some studies have described specific vocalisation types for this species; however, there is still no complete description of its vocal repertoire. Thus, this study aimed to describe the vocal repertoire of a group of S. libidinosus living in theParque Nacional de Brasília, a protected area in the Cerrado area of Central Brazil. We carried out focal samplings and recording of vocalisations of members of an S. libidinosus troop in different behavioural contexts. The call analyses revealed 25 different types of vocalisations, and each call presented significant structural variation. We grouped these vocalisations according to the context of the emission or acoustic structure into the following categories: contact calls (contact note, infant babbling, trill, teeth- and lip-smacking, and sirena); foraging calls (chihui, grgr, and patinado); whistle series (food-associated, long-distance, and intergroup encounter); aggressive calls (aggressive contact note, ascending rapid staccato, cough cough, and pip); calls in response to aggression (scream, squeal, and pulsed scream), sexual display calls (chuck and raspy oestrous call), and stress-related calls (alarm call/bark, hiccup, hip, double hip, and wah wah). S. libidinosus presented a very rich vocal repertoire, revealing a pattern consistent with the repertoire of other capuchin monkey species. This is the first comprehensive description of the S. libidinosus vocal repertoire and highlights the complexity of neotropical primate communication.

Diverse patterns of responsiveness to fine temporal features of acoustic signals in a temperate austral forest frog, Batrachyla leptopus (Batrachylidae)

ABSTRACT Phonotactic female and vocal male responses of frogs to advertisement calls have been shown to encompass broader ranges than those of variation of natural mate-attracting signals. Anuran aggressive calls contribute to expand the range of sound features significant for communication. Evoked vocal responses (EVRs) of males of Batrachyla leptopus to synthetic advertisement calls and variants with different temporal features altered parametrically were studied to assess their correspondence with features of natural signals. Frogs responded to stimuli differing in note rate with vocal patterns that depended on the design of the synthetic sounds: lower call rates were obtained with stimuli composed of notes with linear rise-fall times deviating from the average of this parameter for natural calls. However, opposite results were obtained with stimuli composed of sinusoidally amplitude-modulated notes. Calls of longer duration resembling aggressive calls were emitted in response to low note rate sinusoidal stimuli. Stimuli with note durations above and below the natural average, stimuli having low pulse rates and a continuous tone also elicited longer calls of aggressive type. These patterns relate the vocal responses recorded to recognition of conspecific and heterospecific advertisement and aggressive calls, as well as to novel signal features.

Vocal learning in Savannah sparrows: acoustic similarity to neighbours shapes song development and territorial aggression

Vocal learning is a biologically rare adaptation that underpins both human language and the songs of songbirds. The adaptive value of vocal learning in birds is still poorly understood, but a growing body of literature suggests that vocal learning allows songbirds to gain a fitness advantage by adopting songs that are structurally similar to the songs of individuals in neighbouring breeding territories. In this study, we investigate patterns of song development, acoustic similarity, and territorial aggression in Savannah sparrows, Passerculus sandwichensis. Four years of field data reveal that Savannah sparrows routinely overproduce songs during development; more than half of young males sang more than one song type early in their first breeding season, before their repertoire underwent attrition to a single song that males maintained throughout the remainder of their lives. We also found that the attrition of song types is a selective process, with males retaining songs that are similar to the songs of their territorial neighbours. Males that sang songs that were more similar to their neighbours may have faced lower levels of territorial aggression, as indicated by lower numbers of aggressive calls. Our results provide support for the hypothesis that vocal learning in songbirds allows animals to produce songs that match territorial neighbours, possibly providing a benefit in terms of decreased aggression during territorial defence.

A community context for aggression? Multi-species audience effects on territorial aggression in two species of Paridae.

Territorial aggression in birds is widely observed and is commonly linked to sex, age, body size, physiology, seasonal cues, food resource, urbanization, and a variety of social contexts including conspecific audience effects. However, little is known about the heterospecific audience effects on territorial aggression.Here, we address an emerging idea that heterospecific audience effects may be pervasive influences in the social lives of free‐living birds. We tested the hypothesis that the composition, number, and relative body size of heterospecific audiences observing an aggressive contest will influence the response probability and intensity of aggression displayed.We subjected two Paridae species, tufted titmouse (TUTI, Baeolophus bicolor) and Carolina chickadee (CACH, Poecile carolinensis), to playbacks of aggressive calls during a breeding season in north‐central Florida. At widely spaced playback sites (N = 134) in woodland habitats, we characterized the makeup of heterospecific audiences, aggression type (intra vs. interspecific territoriality), local population density, and various environmental factors (tree density, wind speed, and noise level) that are likely to influence territorial aggression.We found that the presence of heterospecific audiences increased TUTI aggression levels and that both parids were more likely to respond to playback stimuli when their audiences had higher heterospecific diversity (more heterospecific individuals and species). We also found TUTI were more likely to respond when CACH were present but not vice versa.In conclusion, we found evidence that heterospecific audiences significantly influenced the metrics of territorial aggression of free‐living animals and we suggest that the definition of audience effects on the behavior of free‐living animals be expanded to incorporate heterospecific audiences.

How long does it take to know a species? Redescription, vocalization, and chigger mites infestation pattern in the centenary emBrachycephalus/em emgarbeanus/em (Anura: Brachycephalidae).

Although we celebrate the centennial of Brachycephalus garbeanus' discovery, little progress has been done on understanding this species' biology apart from a few morphological and ecological studies, which includes its redescription based on three specimens from the type-series, microhabitat use, sexual dimorphism in body size, and feeding habits. This species is endemic to the Serra dos Órgãos Mountain range, in the state of Rio de Janeiro, southeastern Brazil. Here we redescribe B. garbeanus based on a wide sampling, including its advertisement and aggressive calls, and also the chigger mites infestation pattern. The advertisement call is longer than 25.8 s with pulsed notes series emitted at an average rate of 2.3 notes/s and 14.1 pulses/s; long inter-note interval with 320 ms; notes with distinctly short pulses (1 to 16 ms); low dominant frequency for this genus (3.0-5.4 kHz) and presence of four harmonics. This species is often parasitized by chigger mites of Hannemania, with a prevalence of infection of 67%, mainly affecting the ventral body surface. Females had a higher prevalence of parasites than males and there was no correlation found between the size of specimens and the number of parasites. Our study, provides an important and overdue taxonomical contribution, including a large amount of novel information for B. garbeanus.

Do male Boana goiana (Lutz, 1968) (Anura: Hylidae) discriminate between the calls of neighbours and strangers?

Abstract Neighbour-stranger discrimination is an important mechanism in social behaviour, as it allows the individual to avoid the high energetic costs of repeated agonistic interactions with neighbours. In some anuran species, the owners of territories respond more aggressively towards strangers than neighbours. Here, we investigated whether gladiator frog, Boana goiana, males discriminate between neighbours and strangers. This is a lek-breeding species; therefore, it does not defend fixed territories which are associated with a specific resource. We conducted a playback field experiment with a repeated-measures design, based on three treatments: (i) neighbour’s call in initial position, (ii) stranger’s call in initial position, and (iii) neighbour’s call in new position. We did not observe any systematic modification in the acoustic properties (call duration, dominant frequency, repetition rate) of the advertisement and short aggressive calls of B. goiana males given in response to our playback treatments. Our results indicate that B. goiana males do not exhibit vocally mediated ‘dear enemy’ relationships. We discuss the possible ecological and social factors that may have impeded the evolution of ‘dear enemy’ relationships in this species.

Broad spectrum blast resistance alleles in newly developed Malaysian rice (Oryza sativa L.) genotypes

Rice blast, caused by Magnaporthe oryzae, is a destructive disease. A total of 23 rice genotypes, were screened using a set of 51 simple sequence repeats SSR/ InDel markers and 51 single nucleotide polymorphic (SNP) markers to evaluate the sequence variation. Six newly identified Malaysian isolates of M. oryzae were used for blast screening. The resistant genotypes, consisting of Pongsu Seribu 2, O. rufipogon accessions, Tetep and IR64 had a resistant disease score of 2/3 showing minimal symptoms of blast. In contrast, Mahsuri and MR264 were the most susceptible and had a disease score of 5. In total, 11 sequence variations and two putative haplotype blocks, were observed in the SNP data representing Pi54 and Pita. The SNPs for Pita and Pi54 revealed the presence of resistant alleles that generated reproducible and aggressive calls based on the Sequenom data, but when screened with SSR and INDel markers showed poor correspondence to phenotype effects. Therefore, SNPs for Pi54 and Pita were found to be the most reliable for marker-assisted selection. The blast-resistant alleles identified in this study indicate that they are involved in the defence response against diverse isolates and play a role in putative broad spectrum resistance.

Function analysis of the calls of Dendropsophus microps of the Campos do Jordão State Park, São Paulo, Brazil

In this study, we describe the calls emitted by Dendropsophus microps, a species of frog in the family Hylidae, in Serra da Mantiqueira, Campos do Jordão, São Paulo, Brazil, and evaluate their functions in the social context using playback experiments. Between October 2016 and November 2017, 15 males of D. microps were recorded. Six hundred and five calls were analyzed and the existence of five types of call compositions was verified: simple call “A normal”; compound call “Af”; shorter “A” call + longer “A” call; “A + Af” calls; and simple call “B”; demonstrating the presence of compound calling in the vocalization structure. One thousand, six hundred and seventeen calls were recorded during the playback experiment in response to the 5 previously constructed stimuli. The “B” call was the most emitted in response to stimuli. The “A”, “Af”, “AA” and “AAf” stimuli caused visual signaling. We recorded a series of 4 to 5 “A” calls during agonistic interactions. Call "B" was identified as an advertisement call and calls "A", "Af", "AA" and "AAf" as aggressive calls. The presence of visual communication in addition to the acoustic communication of these individuals was also observed. The findings increase knowledge of the calling repertoire of this species and can be used in the future in other behavioral and taxonomic studies.