Does vocal learning accelerate acoustic diversification? Evolution of contact calls in Neotropical parrots

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open‐ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life‐long vocal learning.     

Body size correlates negatively with the frequency of distress calls and songs of Neotropical birds

ABSTRACT The allometric relationship between body size and song frequency has been established in previous studies of temperate and tropical bird communities. However, the relationship between body size and the frequency of distress calls has been examined in only one study of temperate birds. We examined size‐frequency relationships in the distress calls and songs of a Neotropical bird community in northwestern Costa Rica. In 2008 and 2009, we recorded distress calls and determined the body mass of 54 mist‐netted birds representing 38 species, 35 genera, and 14 families. We obtained songs for these same species from sound libraries and commercially available compact discs. For each vocalization, we measured minimum frequency and frequency of maximum amplitude. Larger birds produced lower‐frequency distress calls and songs than smaller birds. Phylogenetically controlled analyses revealed that the frequency of maximum amplitude was negatively correlated with body mass for both distress calls and songs. Minimum frequency was negatively correlated with mass for distress calls, but not songs. Our analyses suggest that the influence of phylogeny on the relationship between frequency characteristics and body size is modest. Pair‐wise comparisons across 37 species revealed that distress calls and songs had similar minimum frequencies, but songs had significantly lower frequencies of maximum amplitude than distress calls. This difference may arise from differences in signal function. Lower‐frequency sounds should transmit farther through forest habitats and songs must often transmit longer distances to reach their intended audience than distress calls. Our results support the general theory that body size is negatively correlated with the frequency of acoustic signals by demonstrating that this pattern holds true for both distress calls and songs in a Neotropical bird community.     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

The effect of body size and habitat on the evolution of alarm vocalizations in rodents

When confronted with a predator, many mammalian species emit vocalizations known as alarm calls. Vocal structure variation results from the interactive effects of different selective pressures and constraints affecting their production, transmission, and detection. Body size is an important morphological constraint influencing the lowest frequencies that an organism can produce. The acoustic environment influences signal degradation; low frequencies should be favoured in dense forests compared to more open habitats (i.e. the ‘acoustic adaptation hypothesis’). Such hypotheses have been mainly examined in birds, whereas the proximate and ultimate factors affecting vocalizations in nonprimate mammals have received less attention. In the present study, we investigated the relationships between the frequency of alarm calls, body mass, and habitat in 65 species of rodents. Although we found the expected negative relationship between call frequency and body mass, we found no significant differences in acoustic characteristics between closed and open‐habitat species. The results of the present study show that the acoustic frequencies of alarm calls can provide reliable information about the size of a sender in this taxonomic group, although they generally do not support the acoustic adaptation hypothesis.     

Call Characteristics of Two Sympatric and Morphologically Similar Tree Frogs Species,Polypedates megacephalus and Polypedates mutus(Anura: Rhacophoridae), from Hainan,China

Anuran calls are usually species-specific and therefore valued as a tool for species identification. Call characteristics are a potential honest signal in sexual selection because they often reflect male body size. Polypedates megacephalus and P. mutus are two sympatric and morphologically similar tree frogs, but it remains unknown whether their calls are associated with body size. In this study, we compared call characteristics of these two species and investigated any potential relationships with body size. We found that P. megacephalus, males produced six call types which consisting of three distinct notes, while P. mutus males produced five types consisting of two types of notes. Dominant frequency, note duration, pulse duration, and call duration exhibited significant interspecific differences. In P. megacephalus, one note exhibited a dominant frequency that was negatively correlated with body mass, snout-vent length, head length, and head width. In P. mutus, the duration of one note type was positively correlated with body mass and head width. These differences in call characteristics may play an important role in interspecific recognition. Additionally, because interspecific acoustic variation reflects body size, calls may be relevant for sexual selection. Taken together, our results confirmed that calls are a valid tool for distinguishing between the two tree-frog species in the field.     

Female Preferences for Call Traits and Male Mating Success in the Neotropical Frog Physalaemus enesefae

Female preferences for male call traits may affect male mating success and the evolution of exaggerated secondary sexual traits. We used phonotaxis experiments to examine female preferences in the frog Physalaemus enesefae in relation to variation in male call duration, dominant frequency, intercall interval and amplitude (dB SPL). Females preferred long calls, low and average dominant frequency calls, short intercall intervals and more intense calls. We compared the patterns of female preferences with those of acoustic variation among males to test the prediction that properties with low within‐male variation are associated with stabilizing or weakly directional female preferences, whereas properties with high within‐male variation are associated with directional preferences. Females had weakly directional preferences for the dominant frequency of the call and strongly directional preferences for call duration and call rate. We also determined whether the temporal relationship between calls influenced preferences based on the dominant frequency of the call. Preferences for low‐frequency over high‐frequency calls disappeared when calls partially overlapped. Females preferred the leading call regardless of its dominant frequency. We also investigated mating patterns in the field. There was size‐assortative mating, as male and female body sizes snout‐vent length (SVL) were positively correlated. In addition, differences in the frequency distributions of body length (SVL) between mated and unmated males approached significance; lower SVL classes were underrepresented among mated males. These patterns may reflect female preferences for lower dominant frequency calls, as there is a negative correlation between male mass and the dominant frequency of the call.     

Anatomical bases of sex‐ and size‐related acoustic variation in herring gull alarm calls

The hypothesis that anatomical or physiological factors can constrain the production of vocalizations is supported by an increasing number of examples from a range of taxa, where acoustic variation is related to sex, body‐size or condition. In this study, we combine anatomical and acoustic investigations in herring gulls Larus argentatus to 1) identify co‐variation between sex, body size and the dimensions of the vocal apparatus and 2) test the possible effect of this co‐variation on interindividual variation in the acoustics of alarm calls. We found that the vocal apparatus was sexually dimorphic, with males having longer trachea and bigger vibratile membranes than females. We also identified a relationship between the head–bill length – a secondary sexual trait – and the length of the trachea in males only. However, we failed to identify corresponding sex‐ and body‐size related variation in the acoustic components of alarm calls. We suggest that this absence of a relationship between anatomical and acoustic dimensions may reflect the lack of biomechanical constraints exerted during the production of alarm calls, and that such relationships are more likely to be expressed in this species’ sexual calls, whose production is characterised by more pronounced, ritualised postures that are more likely to highlight inter‐individual size variation.     

Do male hoots betray parasite loads in Tawny Owls?

Bird song structure may honestly reveal the health and vigour of individual males to potential mates and competitors. If this is the case then song may reflect the level of parasitic infections in males. We initially examined the relationship between blood parasite infections and the time taken to respond by 22 male Tawny Owls to a broadcast hoot. We then examined the call structure (total length and frequency) in relation to parasite infection, an index of owl condition and an index of food abundance. Owls with higher parasite loads responded more slowly to an intruder, although this relationship was not significant once condition and vole abundance were controlled for. We found no relationship between call length and any of the measured variables. However, the high frequency and the range of frequencies used in calls decreased with increasing parasite load. Thus, there was the potential for individuals to assess male parasite load from the speed of response and the structure of the call. Experimental tests of these relationships are now required.     

The evolution of vocalisations in the genus Corvus: effects of phylogeny, morphology and habitat

In this study we investigated the phylogenetic, morphological and ecological factors affecting the caw calls of 28 species of the genus Corvus, spanning the worldwide range of the taxon. The three phylogeographic groups identified by Goodwin (1986, Crows of the World, British Museum (Natural History), St Edmudsbury Press, Bury St Edmunds), i.e. the American stock, the Palearctic-African stock and the Oriental-Australian stock, were differentiated by some of the acoustic features of their calls, suggesting that historical factors may have played an important role in the evolution of vocalisations in this group. To assess the effects of morphology (body size and bill length) and environment (open vs. closed habitat) and to simultaneously take into account the phylogenetic effects, we used the phylogenetically independent contrast method. This manner of analysis revealed that body size was important in shaping the acoustic attributes of the caw call, as it influenced two temporal and two spectral variables, whereas the effect of bill length was far weaker. Notably, our results did not confirm the negative correlation between call frequency and body size that resulted in a phylogeny-free analysis of the same data in many studies on passerines. Larger Corvus species, in fact, utter calls with higher fundamental frequency than those of smaller species. Hence, these results show that incorporating phylogeny in analyses can substantially alter the conclusions reached by studies carried out with non-phylogenetic approaches. The acoustic environment, considered one of the most important forces driving the evolution of vocalisations in passerines, slightly influenced only two acoustic parameters in the Corvusgenus, call fundamental frequency and duration of pulsed units, both of which increased in the calls of forest species.     

Morphology, echolocation and foraging behaviour in two sympatric sibling species of bat (Tylonycteris pachypus and Tylonycteris robustula) (Chiroptera: Vespertilionidae)

We studied the wing morphology, echolocation calls, foraging behaviour and flight speed of Tylonycteris pachypus and Tylonycteris robustula in Longzhou County, South China during the summer (June–August) of 2005. The wingspan, wing loading and aspect ratio of the two species were relatively low, and those of T. pachypus were lower compared with T. robustula . The echolocation calls of T. pachypus and T. robustula consist of a broadband frequency modulated (FM) sweep followed by a short narrowband FM sweep. The dominant frequency of calls of T. pachypus was 65.1 kHz, whereas that of T. robustula was 57.7 kHz. The call frequencies (including highest frequency of the call, lowest frequency of the call and frequency of the call that contained most energy) of T. pachypus were higher than those of T. robustula , and the pulse duration of the former was longer than that of the latter. The inter-pulse interval and bandwidth of the calls were not significantly different between the two species. Tylonycteris pachypus foraged in more complex environments than T. robustula , although the two species were both netted in edge habitats (around trees or houses), along pathways and in the tops of trees. Tylonycteris pachypus flew slower (straight level flight speed, 4.3 m s⁻¹) than T. robustula (straight level flight speed, 4.8 m s⁻¹). We discuss the relationship between wing morphology, echolocation calls, foraging behaviour and flight speed, and demonstrate resource partitioning between these two species in terms of morphological and behavioural factors.     

Vocal cooperation between the sexes in Little Spotted Kiwi Apteryx owenii

Sexual call dimorphism in birds is usually associated with sexual size dimorphism. Departures from this relationship can be used to infer call function, but research into inter‐sexual call differences, as with song function in general, has been restricted by a bias towards male passerines. The nocturnal and flightless New Zealand kiwi (Apterygidae) are acoustically similar but taxonomically and ecologically very different from other birds, so provide a contrast in exploring avian call function and evolution. However, kiwi acoustic ecology is poorly understood, with the calls of only one of the five kiwi species spectrally described, and acoustic differences between the sexes virtually unknown. We conducted the first bioacoustic study of Little Spotted Kiwi Apteryx owenii, and assessed sexual call dimorphism in this species. There were significant inter‐sexual differences in call temporal and frequency characteristics that were not related to size dimorphism. Contribution to duets and variation in temporal structure with call context also differed between the sexes. We suggest that these differences indicate divergent call function, with male calls more suited for territory defence, and female calls for pair contact. There was a striking lack of overlap in the frequency spectrum distributions of male and female calls, which was also unrelated to size and was further emphasized by the presence of formants in female calls. We propose that this provides evidence for inter‐sexual acoustic cooperation in call frequency, of a type which to our knowledge has not previously been described in birds. This may result from selection for enhanced joint resource defence in kiwi.     

澳大利亚Floreana岛达尔文小树雀喙型与其鸣唱的不相关性

鸟类鸣唱的功能通常是吸引配偶,对于建立繁殖隔离也是非常重要的。现有的研究认为鸟类鸣唱表演可能受到鸟类喙型变化的影响。达尔文鸣雀是一类用来验证喙型和鸣唱表演关系的模型物种,前人的研究认为较低的元音演奏与更大的喙相关。本文用在Floreana岛屿生活的达尔文小树雀(Camarhynchus parvulus)来验证喙型和元音演奏的关系。结果显示,喙型大小与元音演奏之间无相关性。这个发现与过去对小树雀中的研究结果相似,但却与达尔文鸣雀中更大体型的鸟类研究结果相反。讨论了研究结果在物种的生态分化和生态变异之间的前后关系。     

Intraspecific variation in advertisement call characteristics and acoustic strategies among male forest green tree frogs

Frogs are a representative taxon that use advertisement calls to aid in reproduction. In most frog species, calls vary with body size, and allometric constraints between body size and call frequency have been widely reported among anuran species. Although this variation is an important driver of sexual selection in frogs, male advertisement call strategies may also vary according to body size. In this study, we conducted playback experiments on the male forest green tree frog (Zhangixalus arboreus) to determine whether male advertisement call characteristics and strategies vary according to body size and the amplitude of intraspecific chorus noise. The results indicated that the calls of larger individuals are louder and lower than those of smaller ones, who call more frequently; moreover, the calls become lower, and the number of calls decreases, as noise levels increase. These findings suggest that forest green tree frog emits lower calls or refrains from calling when chorus noise increases, and that intraspecific variation in advertisement call characteristics can induce different strategies in response to chorus noise. Because advertisement call variation with body size is common among frog species, intraspecific variation in male advertisement call strategies may also be a common phenomenon.     

Song convergence in multiple urban populations of silvereyes (Zosterops lateralis)

Recent studies have revealed differences between urban and rural vocalizations of numerous bird species. These differences include frequency shifts, amplitude shifts, altered song speed, and selective meme use. If particular memes sung by urban populations are adapted to the urban soundscape, "urban-typical" calls, memes, or repertoires should be consistently used in multiple urban populations of the same species, regardless of geographic location. We tested whether songs or contact calls of silvereyes (Zosterops lateralis) might be subject to such convergent cultural evolution by comparing syllable repertoires of geographically dispersed urban and rural population pairs throughout southeastern Australia. Despite frequency and tempo differences between urban and rural calls, call repertoires were similar between habitat types. However, certain song syllables were used more frequently by birds from urban than rural populations. Partial redundancy analysis revealed that both geographic location and habitat characteristics were important predictors of syllable repertoire composition. These findings suggest convergent cultural evolution: urban populations modify both song and call syllables from their local repertoire in response to noise.     

Differences in songflight calls and social calls between two phonic types of the vespertilionid bat Pipistrellus pipistrellus

The pipistrelle ( Pipistrellus pipistrellus ) occurs as two phonic types in Britain, its echolocation calls falling into two distinct frequency bands, with mean frequencies of maximum energy at 55 kHz and 46 kHz. These are termed the 55 kHz and 45 kHz phonic types here for simplicity. Songflight calls produced by males in the mating season, probably to attract females, differed between the two phonic types in the number of components in the calls and the call parameters measured. Songflight calls of the 55 kHz phonic type, which generally consisted of three components, were of higher frequencies than those of the 45 kHz phonic type, usually of four components. There were also significant differences in call parameters among individuals. A discriminant analysis of songflight calls classified 100% of individuals to the correct phonic type. The relationships between echolocation call frequency and songflight call frequency differed significantly between phonic types. Social calls produced during flight also differed between phonic types, in the number of components and call parameters measured. Social calls were compared to songflight calls of each phonic type. Social calls of the 55 kHz phonic type did not differ significantly from songflight calls; there were small but significant differences between the two types of calls of the 45 kHz phonic type. The study provides support for the hypothesis that the phonic types should be treated as sibling species. If songflight calls are used for mate choice, the differences may allow reproductive isolation between the two phonic types. The functions of songflight calls and social calls need to be investigated through experimental studies to explain the implications of the differences between phonic types.     

Song characteristics track bill morphology along a gradient of urbanization in house finches (<Emphasis Type="Italic">Haemorhous mexicanus</Emphasis>)

Introduction

Urbanization can considerably impact animal ecology, evolution, and behavior. Among the new conditions that animals experience in cities is anthropogenic noise, which can limit the sound space available for animals to communicate using acoustic signals. Some urban bird species increase their song frequencies so that they can be heard above low-frequency background city noise. However, the ability to make such song modifications may be constrained by several morphological factors, including bill gape, size, and shape, thereby limiting the degree to which certain species can vocally adapt to urban settings. We examined the relationship between song characteristics and bill morphology in a species (the house finch, Haemorhous mexicanus) where both vocal performance and bill size are known to differ between city and rural animals.

Results

We found that bills were longer and narrower in more disturbed, urban areas. We observed an increase in minimum song frequency of urban birds, and we also found that the upper frequency limit of songs decreased in direct relation to bill morphology.

Conclusions

These findings are consistent with the hypothesis that birds with longer beaks and therefore longer vocal tracts sing songs with lower maximum frequencies because longer tubes have lower-frequency resonances. Thus, for the first time, we reveal dual constraints (one biotic, one abiotic) on the song frequency range of urban animals. Urban foraging pressures may additionally interact with the acoustic environment to shape bill traits and vocal performance.

     

CONFERENCE ANNOUNCEMENTS

ABSTRACT

In most mammals, adults produce relatively low frequency vocalizations compared to those of juveniles. This rule is not maintained however at least in four species of ground squirrels, whose juveniles call at the adult's fundamental frequency. These findings have been obtained however with separate sets of juveniles and adults and no data is available concerning the ontogeny linked to these differences. Here we analyze the acoustic structure of alarm calls of the same Yellow Spermophilus fulvus and Speckled S. suslicus ground squirrel individuals, recorded as pups and as adults after hibernation. We found the fundamental frequencies of adults within the same frequency ranges as those of pups, in spite of the significant difference in body mass. In ground squirrels, severing the relationship between body size and call frequency removes some vocal cues to age. We discuss some functional hypotheses advanced to explain manipulations with fundamental frequencies in ground squirrels and other animals, and suggest the lack of data for discussing the mechanisms of such vocal tuning.     

Song Frequency Does Not Reflect Differences in Body Size among Males in Two Oscine Species

Large animals, having large vocal organs, produce low sound frequencies more efficiently. Accordingly, the frequency of vocalizations is often negatively related to body size across species, and also among individuals of many species, including several non‐oscine birds (non‐songbirds). Little is known about whether song frequency reveals information about body size within oscine species, which are characterized by song learning and large repertoires. We asked whether song frequency is related to body size in two oscines that differ in repertoire size: the dark‐eyed junco (Junco hyemalis) and the serin (Serinus serinus). We also asked whether the extent to which receivers sample repertoires might influence the reliability of their assessment of body size. We found that none of the frequency traits of song that we investigated was related to male body size, nor did more extensive sampling of repertoires lead to any relationship between frequency and body size. Possible reasons for these results are the small range of variation in size within species, or the elaborate vocal physiology of oscines that gives them great control over a wide frequency range. We discuss these results as they relate to female preferences for high‐frequency song that have been previously reported for oscine species.     

The distribution and habitats of crossbills Loxia spp. in Britain, with special reference to the Scottish Crossbill Loxia scotica

A study was carried out, primarily in northern Scotland, to relate bill and wing measurements to diagnostic calls of crossbill species, and thereby use the calls to describe the distributions and habitats of the different species. Bill depth and wing length measurements from museum specimens and live‐trapped birds were used to describe the size categories. Almost all measurements of crossbills from England were similar to measurements of Common Crossbills from Fennoscandia. Museum specimens showed that crossbills in northern Scotland between 1822 and 1990 were a combination of Common Crossbills, birds which were intermediate between Common and Parrot Crossbills (Scottish Crossbills), and perhaps a few Parrot Crossbills. However, catches of crossbills between 1995 and 2000 showed that Parrot Crossbills (based on bill and wing measurements) were present at some sites in the Highlands. Recordings of flight calls and excitement calls of birds of known bill sizes allowed a classification of crossbills according to call types. Four different flight calls (referred to here as types 1–4) and five excitement calls (types A–E) were recognized. A sample of small‐billed birds, thereby identified as Common Crossbills, indicated that there were three groups of Common Crossbills: those giving type 1 flight calls and type A excitement calls (1A), type 2 flight calls and type B excitement calls (2B), and type 4 flight calls and type E excitement calls (4E). Large‐billed birds identified as Parrot Crossbills gave mainly type 2 flight calls and type D excitement calls. Birds with intermediate bill depths (Scottish Crossbills) gave type 3 flight calls and type C excitement calls. Distributions based on calls showed that 1A Common Crossbills were widespread in Scotland but the other types of Common Crossbill were rare. Parrot Crossbills were found in a few localities in the Highlands, and Scottish Crossbills (defined as those giving type 3 flight calls and type C excitement calls) were restricted to the northern and eastern Highlands. Scottish Crossbills and 1A Common Crossbills had overlapping distributions, and overlapped greatly in the types of forests they used between January and March when the Scots Pine cones were still closed. However, Scottish Crossbills were more frequently associated with stands containing Scots Pine compared with Common Crossbills.     

A Comparative Study of the Songs and Alarm Calls of some Parus Species

Titmice vocalizations are presented with a view to examining variation within and between species. Analyses are derived from field recordings of British Parus species, and from available disc recordings. Spectrographic and oscillographic analyses are made of territorial song and alarm calls. The extent of song divergence and alarm call convergence is illustrated and discussed in addition to data on variation of these calls within species. Some brief notes on field behaviour are included and methods of sound production in birds discussed.