Seasonal and diurnal patterns of population vocal activity in avian brood parasites

Patterns of vocal activity may involve information about vocalizations themselves as well as their function. In birds, vocal activity at the individual and population level is generally closely associated with breeding cycles, reaching the peak during territorial and mating competition, and decreasing with the onset of egg incubation and chick feeding. However, little is known about patterns of vocal activity in avian brood parasites that have unusual breeding cycles without parental care. Using passive acoustic monitoring, we determined the seasonal and diurnal patterns of population vocal activity in two avian brood parasites: the Common Cuckoo Cuculus canorus and the Lesser Cuckoo C. poliocephalus. We found that both species and both sexes showed a similarly highly structured pattern of seasonal vocal activity, reaching a sharp peak in the early breeding season when birds compete for territories and mates, although males sang more frequently than females. Likewise, the diurnal patterns of vocal activity were similar in both species and both sexes of cuckoos, with peak activity occurring around dawn. Nocturnal calls by male cuckoos were also detected in both species, but only in the early breeding season. Collectively, the observed patterns of population vocal activity may suggest that the absence of parental care may not extend the period of vocal activity in these two species of brood parasites.     

大鹰鹃鸣声的日节律

鸟类的鸣唱具有吸引配偶和保卫领域的功能,多为雀形目雄性鸟类发出,在其婚配、繁殖中起重要作用。非雀形目鸟类缺乏内鸣肌,发出的声音较为单调。但杜鹃科(Cuculidae)等少数非雀形目鸟类,利用鸣叫来吸引异性和宣示领域,功能上类似雀形目鸟类的鸣唱。鸟类在繁殖期面临觅食等基本生理活动与求偶行为的时间权衡。而鸣唱是雄性鸟类在繁殖期耗能较多的求偶行为,鸣唱的活跃程度受到外界环境和鸟类自身习性的影响。通过研究鸟类鸣声的日节律,有助于了解鸟类对生活史策略的响应。本研究于2016年和2017年鸟类繁殖季在北京小龙门森林公园(40°00′N,115°26′E)进行。2016年和2017年在大鹰鹃(Hierococcyx sparverioides)活动区利用录音机(美国Wildlife Acoustics公司,型号SM4)分别录制了3 d和43 d的录音。通过Kaleidoscope Pro 4.0.3软件(美国Wildlife Acoustics公司),量化录音并提取反应大鹰鹃鸣声特征的参数,进而自动识别出录音中大鹰鹃的鸣声。在优化识别条件后,对大鹰鹃鸣声识别的正确率可以达到60.26%,探测率可以达到44.71%。发现大鹰鹃有两个鸣叫的高峰,一个在3:00时,另一个在19:00时。与同域分布的其他鸟类相比,大鹰鹃鸣声的高峰时段持续的时间更长,且具有夜间鸣叫的特点。结合大鹰鹃的生活史,我们对其鸣声日节律进行了讨论。     

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds' bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting that the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.     

Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds

Many laboratories are conducting research using songbirds as their animal model. In particular, songbirds are widely used for studying the behavioural and neural mechanisms underlying vocal learning. Many researchers use wild-caught birds to conduct this research, although few studies of behaviour have been conducted to determine the effects of captive housing on these species. We investigated the vocal production pattern of wild-caught black-capped chickadees (Poecile atricapillus) over an entire season in laboratory housing. We documented the frequency of production of four vocalizations (fee-bee song, chick-a-dee calls, dee calls, and gargle calls) across seasons and diurnal pattern and compared the observed pattern of laboratory vocalizations to those previously observed and reported in the wild. Laboratory-housed chickadees had seasonal and diurnal vocal production shifts that were related to both photoperiodic changes (season) and diurnal pattern. For instance, there was significantly more fee-bee song in the spring than summer, autumn, and winter with the most fee-bee song occurring at spring dawn as seen in the wild. Our results also confirmed that the general pattern of vocalizations was consistent between wild and laboratory populations, with no significant differences for either the seasonal or diurnal pattern of fee-bee song production between populations. Differences between settings were observed in the pattern of chick-a-dee calls at dawn and sunset between field and laboratory populations. However, differences in the quantity of vocalization types between laboratory and wild populations suggest that housing conditions are influencing the normal vocal behavioural patterns.     

Larger body size on islands affects silvereye Zosterops lateralis song and call frequency

Differences in song repertoires and characteristics of island and mainland populations of the same avian species are usually explained by dispersal, cultural evolution and/or habitat differences. The influence of morphology is often overlooked, even though island populations are frequently morphologically distinct from mainland populations, and morphology could affect vocalizations. I compared morphological features, songs, contact calls and alarm calls of six isolated island populations of silvereye Zosterops lateralis with those of two mainland populations to examine whether differences between mainland and island vocalizations were consistent across vocalization types, and whether these differences could be linked to morphological differences. Vocalizations were lower in frequency on islands. Island individuals were larger (both in mass and body structure), and body mass was an important predictor of frequency in contact and alarm calls. I argue that this strong association results from the island rule (islands promote larger body sizes) and cascading effects of morphology on vocalization frequency in this species.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Seasonal plasticity in auditory processing of the envelope and temporal fine structure of sounds in three songbirds

Songs mediate mate attraction and territorial defence in songbirds during the breeding season. Outside of the breeding season, the avian vocal repertoire often includes calls that function in foraging, antipredator and social behaviours. Songs and calls can differ substantially in their spectral and temporal content. Given seasonal variation in the vocal signals, the sender–receiver matching hypothesis predicts seasonal changes in auditory processing that match the physical properties of songs during the breeding season and calls outside of it. We tested this hypothesis in white-breasted nuthatches, Sitta carolinensis, tufted titmice, Baeolophus bicolor, and Carolina chickadees, Poecile carolinensis. We measured the envelope-following response (EFR), which quantifies phase locking to the amplitude envelope, and the frequency-following response (FFR), which quantifies phase locking to the temporal fine structure of sounds. Because songs and calls of nuthatches are amplitude modulated at different rates, we predicted seasonal changes in EFRs that match the rates of amplitude fluctuation in songs and calls. In chickadees and titmice, we predicted stronger FFRs during the spring and stronger EFRs during the winter because songs are tonal and calls include amplitude-modulated elements. In all three species, we found seasonal changes in EFRs and FFRs. EFRs varied across seasons and matched the amplitude modulations of songs and calls in nuthatches. In addition, female chickadees had stronger EFRs in the winter than in the spring. In all three species, FFRs during the spring tended to be stronger in females than in males. We also found species differences in EFRs and FFRs in both seasons; EFRs and FFRs tended to be higher in nuthatches than in chickadees and titmice. We discuss the potential mechanisms underlying seasonality in EFRs and FFRs and the implications of our results for communication during the breeding season and outside of it, when these three species form mixed-species flocks.     

Does Interspecific Eavesdropping Promote Aerial Aggregations in European Pipistrelle Bats During Autumn?

Eavesdropping is a widespread strategy to optimize decision‐making. Bats are interesting models for investigating acoustic information transfer, as they possess a broad vocalization repertoire of echolocation and social calls. Yet, the knowledge of the extent to which eavesdropping plays a role in bat communication is scarce. Here, we examined the vocal and spatial activity patterns of three congeneric bat species (Pipistrellus pipistrellus, P. pygmaeus, P. nathusii, hereafter called pipistrelles) during autumn – their migration and mating season. We hypothesized that pipistrelles utilize information of conspecifics and congenerics to localize stopover sites for mating or other information purposes during migration. We found that bats formed small multispecies aggregations on the wing, suggesting interspecific eavesdropping on feeding buzzes and/or courtship calls could occur among these species. Pipistrelles produced similar proportions of feeding buzzes and social calls at aggregation sites. To test whether pipistrelles respond to the courtship vocalizations of conspecifics and congenerics, we conducted a playback experiment with P. pipistrellus where we presented courtship vocalizations of the three pipistrelle species and as a control, a motif of the noctule bat's song (Nyctalus noctula). Pipistrellus pipistrellus decreased the rate of social calls in response to the broadcast of songs of P. nathusii, yet they tended to increase the rate in response to the playback of their own species. We conclude that interspecific eavesdropping occurs at least between P. pipistrellus and P. nathusii and might thus favour the formation of multispecies aggregations. Our findings provide novel insights into the social behaviour and interspecific communication of a bat community during the season of migration and mating.     

Of Mice,Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other''s pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.     

Male singing behaviour and female presence in the territory in whitethroats Sylvia communis

Unmated male songbirds usually change their vocal behaviour when females enter their territories. Either the males court the females by changing the rate or pattern with which their normal long-ranging full songs are emitted, or they shift to special displays and long- or short-ranging vocalisations. In this study we quantified how female presence and behaviour affect the singing behaviour of male whitethroats. In the presence of a female the male frequently performed song flights, maybe to locate the female before it was courted, with sequences of diving-song displays. The courtship was interrupted by periods of perch songs. Female dscharp calls and short movements made the males initiate or resume courtship, whereas short horizontal jumps made the males intensify their courtship. Overall, the males changed their dual-function song activity in females' presence by emitting fewer perch songs and more flight songs. The quiet diving songs were only emitted during direct courtship of a female. The song types emitted immediately before, during, and after courtship are all highly variable, thus allowing for a quick assessment of the male's song repertoire. The courtship was also interrupted by periods of male woid calling, a call that is known to have a deterring effect on rival males. Bouts of woid calls were usually followed by song flights, again probably to locate the female that might have moved out of sight, or maybe to locate potential rival intruders. The latter was supported by an increased intrusion rate during female presence. Communicated by P. McGregor     

Territorial vocalization in sympatric damselfish: acoustic characteristics and intruder discrimination

Damselfishes are well known for their aggressive, territorial behaviour during which the use of vocalization behaviour has been well documented. However, agonistic acoustic signalling has been understudied in particular when the vocalizations are interspecific. In this study, we characterize and compare the previously undescribed vocalization behaviour of longfin damselfish (Stegastes diencaeus), in an agonistic context, with the closely related and sympatric dusky damselfish (Stegastes adustus). Next, we examined if these congeneric species modulate their vocalizations in a similar pattern to previously described aggressive behaviour patterns. Audio field recordings of territorial males were obtained in response to three separate stimuli: (1) conspecific male damselfish, (2) heterospecific male damselfish and (3) a common intruder, the slippery dick wrasse (Halichoeres bivittatus). The vocal repertoires of both longfin and dusky damselfish comprised the same three distinct call types: chirps, pops and pulse trains. However, temporal measures of the calls showed significant differences between species. Additionally, dusky damselfish were more vocal overall, producing more calls and spending more time calling than longfin damselfish. These responses were stimulus and species dependent, as the two species modulated acoustic response by modulating pulse number based on intruder species. These results suggest that these closely related species of damselfish use vocalization behaviours that are both unique and context dependent.     

Understanding the function of nocturnal song in ovenbirds: males do not countersing at night

Many diurnal bird species vocalize at night, however the function of nocturnal song is, generally, still poorly understood. Previous research has suggested that nocturnal song may serve a social function and is influenced by environmental factors. To test whether males attend to the nocturnal song of conspecifics, we experimentally exposed ovenbirds Seiurus aurocapilla to nocturnal flight songs, and recorded their response both during the night and during the following dawn chorus. We compared latency to song and vocal output before and after playback exposure to determine if males altered their vocalizations in response to exposure to flight songs from an unknown male. We found no evidence of counter singing or change in nocturnal song output, nor a change in vocal output during the dawn chorus following playback exposure. Our results suggest that, in ovenbirds, nocturnal song does not serve as an intraspecific social function. Nocturnal song, through rare, may be significant in the mating systems of some diurnal bird species, and requires additional study.     

Divergence in calls but not songs in the orchard oriole complex: Icterus spurius and I. fuertesi

Birdsong has important functions in attracting and competing for mates, and song characteristics are thought to diverge rapidly during the process of speciation. In contrast, other avian vocalizations that may have non‐reproductive functions, such as calls, are thought to be more evolutionarily conserved and may diverge more slowly among taxa. This study examines differences in both male song and an acoustically simpler vocalization, the ‘jeet’ call, between two closely related taxa, Icterus spurius and I. fuertesi. A previous study comparing song syllable type sharing within and between I. spurius and I. fuertesi indicated that their songs do not differ discernibly. Here we measured 18 acoustic characteristics of their songs and found strong evidence supporting this prior finding. In contrast, we measured 17 acoustic characteristics of jeet calls and found evidence of significant divergence between the two taxa in many of these characteristics. Calls in I. fuertesi have a longer duration, a larger frequency bandwidth, a lower minimum frequency, a lower beginning frequency, and greater levels of both frequency and amplitude modulation in comparison to the calls of I. spurius. In addition, I. fuertesi calls contain two distinct parts, while the calls of I. spurius have only one part. Thus, we find evidence of divergence in the calls of the two taxa but not their songs challenging the widespread assumption that complex bird song evolves more rapidly than other types of vocalizations. Understanding divergence in multiple vocalization types as well as other behavioral, morphological, and molecular traits is important to understanding the earliest stages of speciation.     

Vocal Ontogeny in Neotropical Singing Mice (Scotinomys)

Isolation calls produced by dependent young are a fundamental form of communication. For species in which vocal signals remain important to adult communication, the function and social context of vocal behavior changes dramatically with the onset of sexual maturity. The ontogenetic relationship between these distinct forms of acoustic communication is surprisingly under-studied. We conducted a detailed analysis of vocal development in sister species of Neotropical singing mice, Scotinomys teguina and S. xerampelinus. Adult singing mice are remarkable for their advertisement songs, rapidly articulated trills used in long-distance communication; the vocal behavior of pups was previously undescribed. We recorded 30 S. teguina and 15 S. xerampelinus pups daily, from birth to weaning; 23 S. teguina and 11 S. xerampelinus were recorded until sexual maturity. Like other rodent species with poikilothermic young, singing mice were highly vocal during the first weeks of life and stopped vocalizing before weaning. Production of first advertisement songs coincided with the onset of sexual maturity after a silent period of ≧2 weeks. Species differences in vocal behavior emerged early in ontogeny and notes that comprise adult song were produced from birth. However, the organization and relative abundance of distinct note types was very different between pups and adults. Notably, the structure, note repetition rate, and intra-individual repeatability of pup vocalizations did not become more adult-like with age; the highly stereotyped structure of adult song appeared de novo in the first songs of young adults. We conclude that, while the basic elements of adult song are available from birth, distinct selection pressures during maternal dependency, dispersal, and territorial establishment favor major shifts in the structure and prevalence of acoustic signals. This study provides insight into how an evolutionarily conserved form of acoustic signaling provides the raw material for adult vocalizations that are highly species specific.     

Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren ( Malurus splendens ) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird ( Cracticus torquatus ). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.     

Zebra Finch Mates Use Their Forebrain Song System in Unlearned Call Communication

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which “stack” calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.     

Cues to Androgens and Quality in Male Gibbon Songs

Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers'' attributes.     

An Interactive Playback Experiment Shows Song Bout Size Discrimination in the Suboscine Vermilion Flycatcher (Pyrocephalus rubinus)

Many aspects of the social behaviour of birds are mediated by vocal displays, and variation in song output or song structure conveys different information to receivers. After nest construction begins, when vermilion flycatcher (Pyrocephalus rubinus) females are potentially fertile, males increase their song rate during the dawn chorus. A previous study failed to give evidence that males discriminate among song rates. However, males sing in sequences of songs (song bouts), and an increase in song rate may be achieved by increasing the number of bouts, the number of songs in each bout (bout size) or both. Studying a vermilion flycatcher population in Mexico City, we evaluated whether dawn song rate is related to song bout size or to number of bouts. Bout size correlated with song rate and differed among males. We hypothesized that longer bouts are more threatening signals than shorter ones and predicted a stronger response by males towards the former. We exposed each male to three playback treatments: (1) Long song bout (Long), in which we replied to the male with twice the number of songs he sang in the bout, (2) Short song bout (Short), in which we played half the number of songs sung by the male and (3) Control, this was the same as the Long treatment but we used songs from a related species, the tropical kingbird (Tyrannus melancholicus). Males responded with a higher proportion of calls near the speaker when exposed to the Long treatment than during the Short or Control treatments, indicating that they discriminate among song bouts differing in size, that they may perceive longer bouts as more threatening and that they use calls rather than songs to address threatening situations. Our results suggest that song bout size is a relevant song attribute that conveys information during intrasexual interactions.     

Acoustic structure of vocalization and stapedius muscle activity during vocal development in chickens (Gallus gallus)

The link between stapedius muscle activity and acoustic structure of vocalization was analysed in cocks of age 20–30 to 90–100 days old. The results show that stapedius muscle activation depends on the acoustic structure of vocalization and changes during vocal development. This dependence was observed in spontaneous calls and in vocalizations elicited by stimulating the mesencephalic calling area. In 30-day-old cocks stapedius muscle EMG response is never associated with vocalizations with an acoustic energy content which is always distributed at frequencies higher than 2000 Hz. The coupling between vocalization and stapedius muscle activity begins later, when birds produce vocalizations with acoustic energy shifted towards lower frequencies. Overall, stapedius muscle activity is related to a bird's production of high amplitude low frequencies. These results support the hypothesis that the primary role of the stapedius muscle during normal vocal development is to dampen the amplitude of low frequency energy that reaches the cochlea during vocalization.