Long-tailed Manakins Research Articles

Edge weight variance: population genetic metrics for social network analysis

We present novel metrics for analysis of weighted social networks that focus explicitly on the distribution of edge weights at hierarchical scales from node to egonet to community and to the network as a whole. The formulae are adapted from existing measures, originally developed in the context of population genetics to analyse variance in gene frequencies at different levels of organization. Our metrics, including ‘effective degree’ (by analogy to effective number of alleles), ‘concentration’ (by analogy to the inbreeding coefficient), ‘observed’ and ‘expected edge weight diversity’ (by analogy to observed and expected gene diversity) and F statistics allow one to partition the variance in edge weights among hierarchical levels of organization within networks. They provide a quantitative method for addressing issues as diverse as disease transmission, social complexity, the spread of learned behaviours and the evolution of cooperation. We illustrate the utility of these new metrics by applying them to three empirical social networks: long-tailed manakins, Chiroxiphia linearis, monk parakeets, Myiopsitta monachus, and mountain goats, Oreamnos americanus.

Mating dances and the evolution of language: What’s the next step?

The Darwinian protolanguage hypothesis is one of the most popular theories of the evolution of human language. According to this hypothesis, language evolved through a three stage process involving general increases in intelligence, the emergence of grammatical structure as a result of sexual selection on protomusical songs, and finally the attachment of meaning to the components of those songs. The strongest evidence for the second stage of this process has been considered to be birdsong, and as a result researchers have investigated the existence of various forms of grammar in the production and comprehension of songs by birds. Here, we argue that mating dances are another relevant source of sexually-selected complexity that has until now been largely overlooked by proponents of Darwinian protolanguage, focusing especially on the dances of long-tailed manakins. We end by sketching several lines of research that should be pursued to determine the relevance of mating dances to the evolution of language.

The Song Overlap Null model Generator (SONG): a new tool for distinguishing between random and non-random song overlap

Song overlapping, a behaviour in which an individual begins singing before its counterpart has completed its song, has been the subject of recent debate. Although many studies have suggested that song overlapping functions as a signal, the majority of these studies fail to address the possibility that overlapping is a chance occurrence. Part of the difficulty in determining whether overlap is intentional or accidental lies in the lack of compelling null models for estimating chance levels of song overlap. We have developed the Song Overlap Null model Generator (SONG), a software package for R. SONG uses resampling randomization to predict the expected amount of overlap due to chance, and is applicable to any system in which individuals engage in signalling interactions. To evaluate the effectiveness of SONG, we examined the overlapping behaviour of three avian species: black-capped chickadees (Poecile atricapillus), rufous-and-white wrens (Thryophilus rufalbus) and long-tailed manakins (Chiroxiphia linearis). Our analyses revealed that black-capped chickadees avoided overlapping the songs of playback-simulated intruders, duetting wrens overlapped the songs of their mates and manakins avoided overlapping the duets of their neighbours. We believe that SONG will prove to be a valuable tool for understanding signal timing in songbirds as well as other taxa.

A Controlled Sensing Approach to Graph Classification

The problem of classifying graphs with respect to connectivity via partial observations of nodes is posed as a composite hypothesis testing problem with controlled sensing. An observation at a node is a subset of edges incident to the node on the complete graph drawn according to a probability model, which is a function of a fixed underlying graph. Connectivity is measured through average node degree and is classified with respect to a threshold. A simple approximation of the controlled sensing test is derived and simulated on Erdös-Rènyi graphs to characterize the error probabilities as a function of the expected stopping times. The test is also experimentally validated on a real-world example of the social structure of Long-Tailed Manakins. It is shown that the proposed test achieves favorable tradeoffs between the classification error and the number of measurements. Furthermore, the test outperforms existing approaches, especially at low target error rates. In addition, the proposed test achieves the optimal error exponent.

Structure of male cooperation networks at long-tailed manakin leks

Social networks arise from complex interactions among multiple individuals and affect the emergent properties of groups (e.g. cooperation, disease spread, information transfer, etc.). Cooperation among nonkin is generally predicted to be favoured in structured social networks where individuals primarily interact only with certain individuals. Long-tailed manakins, Chiroxiphia linearis , form lek groups of as many as 15 unrelated males, whose members can attend multiple leks. At each lek, several top-ranked males perform the majority of obligate cooperative courtship displays. We used exponential random graph (ERG) modelling to analyse manakin cooperation networks constructed from 2-year time intervals over a 14-year study period. ERG modelling evaluates how local processes contribute to formation of global social network structure. We found that four local processes of link formation largely explained the overall structure of male manakin cooperation networks: (1) the spatial proximity of birds: males were more likely to cooperate if they primarily displayed at the same or neighbouring leks; (2) social status of birds: males were more likely to cooperate as they moved up the social queue at leks; (3) triad closure: males were more likely to cooperate with a ‘friend of a friend’ than with males with which they did not share a mutual partner; and (4) link persistence: males were more likely to cooperate with males whom they had cooperated with in the past. Other plausible mechanisms, such as selective mixing (the tendency to interact with individuals of similar or dissimilar social status) and preferential attachment by degree (whereby individuals with many social links gain additional links) did not consistently explain the structure of male cooperation networks at leks. These local processes may facilitate cooperation among long-tailed manakins by creating structured social networks in which males interact with only a subset of the population. • We examined formation of cooperation networks in male long-tailed manakins. • We used exponential random graph modelling to assess contributions of local network processes. • Spatial proximity, social status, triad closure and prior partnership affected network formation. • These local network processes may facilitate cooperation among male long-tailed manakins.

Telemetric and video assessment of female response to male vocal performance in a lek-mating manakin

Sexual signals play an important role in mate attraction. In this study, we explore male vocal behavior and female mate attraction in long-tailed manakins, tropical lekking birds where males perform cooperative displays to attract females, and males provide only gametes to choosy females. We monitored female visitation at 37 sites using two techniques: video recordings and automated radiotelemetry. Simultaneously, we used digital recorders to sample male vocal behavior, quantifying vocal output as well as frequency matching and temporal synchrony in male–male duets. We compared male vocal performance to the rate at which females visited male display sites. Video data revealed that both male vocal output and the temporal synchrony of male–male duets were positively related to female visitation, matching our expectations. Telemetry data, in contrast, revealed no such relationship. Our results suggest that telemetry data may yield biased estimates of patterns of female choice, because the tracked females may not adequately represent the pool of potential female visitors to leks. We also demonstrate that male vocal behavior and female visitation vary, in concert, with time of day, peaking in the early morning, with a pronounced drop in the mid-day heat. We compare these results with those of another study, of the same species, in a montane environment with cooler daytime temperatures.

Cooperative courtship display in Long-tailed Manakins Chiroxiphia linearis: predictors of courtship success revealed through full characterization of display

The Pipridae comprise 52 species of manakins with a wide variety of courtship behaviours, ranging from solitary display, to traditional leks, to cooperative display. Long-tailed Manakins (Chiroxiphia linearis) exhibit an exploded lek-breeding system wherein two unrelated males cooperate to perform complex courtship displays for females. Our objectives in this study were to fully characterize the courtship display of Long-tailed Manakins, to evaluate the sequence and stereotypy of the display, and to investigate specific predictors of copulation success. Whereas the display of Long-tailed Manakins has traditionally been divided into two major parts, the hopping display and the butterfly display, we identified and characterized 16 individual display elements within these larger components of the display. We also determined that some aspects of the display are highly structured and stereotypical in performance, such that certain elements of the display are highly likely to be preceded or followed by particular elements. Nevertheless, other aspects of the display were much more flexible in terms of element sequence. We also found that the length and rate of performance of individual display elements were highly variable across displays. We therefore evaluated whether individual elements of the display could predict courtship success. Our results show that a number of highly correlated elements, namely upright postures, bounces, angel flights, and bows, can predict whether a display ends in copulation with a female. This research enhances our understanding of male display behaviour and female choice in Long-tailed Manakins, and may shed some light on the evolution of complex courtship displays in birds.

A Young Manakin Knows His Place: Evidence for an Age‐Graded Dominance Hierarchy Among Long‐Tailed Manakins

AbstractIn lek‐breeding systems where many males gather at display sites, males benefit from the establishment of dominance hierarchies to reduce intrasexual aggression and the associated risk of injuries. Long‐tailed manakins (Chiroxiphia linearis) exhibit an exploded lek‐breeding system wherein the two top‐ranking males at each display site team up to perform elaborate coordinated courtship displays for females. Young males undergo delayed plumage maturation whereby they acquire distinct pre‐definitive plumage patterns each year until they attain definitive plumage in their fifth year. This unique characteristic is thought to have evolved as a status‐signalling mechanism to aid in the establishment of an age‐graded dominance hierarchy in which older males are dominant to younger males. Previous research has shown evidence for such a dominance hierarchy among alpha and beta males; however, the presence of this hierarchy among males of other age classes has never been quantified. In this study, we investigated the presence of an age‐graded dominance hierarchy by determining whether older males direct more aggressive behaviours towards younger males. We also investigated whether status signalling is less clear within age classes than between age classes, by determining whether males within the same age class exhibit more aggression towards each other. We found that older males performed aggressive behaviours towards younger males much more frequently than younger males performed aggressive behaviours towards older males. We also found that some aggressive interactions occurred between males within the same age class more frequently than between males from different age classes. Our study provides some evidence for an age‐graded dominance hierarchy among male long‐tailed manakins of all age classes and also provides some support for the status‐signalling hypothesis. However, further research is needed to conclusively establish the presence of a linear dominance hierarchy among younger male manakins. This research may help us better understand the evolution of complex hierarchical systems in animals.

Calling in an acoustically competitive environment: duetting male long-tailed manakins avoid overlapping neighbours but not playback-simulated rivals

Animals that live in communication range of multiple conspecific receivers have the potential to interfere with their neighbours' signals, or to avoid interference by signalling at different times. We used both an observational and experimental approach to study signal timing in lekking tropical birds. We recorded duetting pairs of male long-tailed manakins, Chiroxiphia linearis, during periods when two neighbouring pairs were calling concurrently, and during playback of a simulated pair of nearby rival males. We used three complementary analytical techniques to evaluate whether birds varied the timing of their duet calls relative to nearby animals: circular statistics, resampling analysis and duty cycle models. Our analyses reveal that long-tailed manakins produce duets with nonrandom timing with respect to the calls of their rivals. During natural bouts of concurrent calling, all three analytical techniques revealed that manakins time their duets to avoid overlap. In response to playback, males showed more variable strategies. Males overlapped duets more during playback than they did under natural conditions and, in some cases, they overlapped playback duets at higher levels than would be expected based on chance. Our study shows that males alter the timing of their calls in response to the vocalizations of others around them, and it uncovers similarities in the acoustic signalling behaviour of lekking birds relative to the better-studied signalling behaviour of territorial birds. We also show that different null models of signal timing yield different insights into animal signalling behaviour.

Long-tailed Manakin (Chiroxiphia linearis)

Long-tailed Manakin (Chiroxiphia linearis)

Chewing lice (Phthiraptera) on manakins (Passeriformes: Pipridae) from Costa Rica, with description of a new species of the genus Tyranniphilopterus (Phthiraptera: Philopteridae)

One hundred and seventy individuals of five species of manakins (Passeriformes: Pipridae) were examined for chewing lice (Phthiraptera) in Costa Rica. Six species of chewing lice were identified. Chewing lice or their eggs were found on 26% individuals (28 positive/109 examined) of Long-tailed Manakins (Chiroxiphia linearis), the most numerous manakin species examined. There were significant differences in prevalences and intensities of infestation between males and females. No lice were found on females (n = 28) compared to 35% (24 positive/69 examined) prevalence in males. In older males, the higher prevalence and mean intensity of infestation was found. Description and illustrations are given for a new species of the genus Tyranniphilopterus Mey, 2004 from Long-tailed Manakin-Tyranniphilopterus toledo Sychra, sp. n. Both sexes of Tyranniphilopterus bruneri (Carriker, 1903) are redescribed. New host records are Long-tailed Manakin and White-collared Manakin (Manacus candei) for Ricinus invadens; White-ruffed Manakin (Corapipo altera) for Ricinus pessimalis; Long-tailed Manakin for Myrsidea andyolsoni. These are the first louse records from Long-tailed Manakin.

Young-boy networks without kin clusters in a lek-mating manakin

I use 10 years of data from a long-term study of lek-mating long-tailed manakins to relate the social network among males to their spatial and genetic structure. Previously, I showed that the network connectivity of young males predicts their future success. Here, I ask whether kinship might shape the organization of this “young-boy network”. Not surprisingly, males that were more socially distant (linked by longer network paths) were affiliated with perch zones (lek arenas) that were further apart. Relatedness (r) among males within the network decreased as social distance increased, as might be expected under kin selection. Nevertheless, any role for indirect inclusive fitness benefits is refuted by the slightly negative mean relatedness among males at all social distances within the network (overall mean r = −0.06). That is, relatedness ranged from slightly negative (−0.04) to more negative (−0.2). In contrast, relatedness in dyads for which at least one of the males was outside the social network (involving at least one blood-sampled male not documented to have interacted with other banded males) was slightly above the random expectation (mean r = 0.05). The slight variations around r = 0 among males of different categories likely reflect dispersal dynamics, rather than any influence of kinship on social organization. Relatedness did not covary with the age difference between males. These results, together with previous results for lack of relatedness between alpha and beta male partners, refute any role for kin selection in the evolution of cooperative display in this lek-mating system.

Do museum specimens accurately represent wild birds? A case study of carotenoid, melanin, and structural colours in long‐tailed manakins Chiroxiphia linearis

Museum specimens continue to be an invaluable resource for taxonomic, systematic, and comparative studies, and are increasingly relied upon for novel research purposes. Evaluating variation in the colour of avian study skins forms the basis for a broad range of research questions, yet few studies have investigated whether the plumage colouration of museum specimens accurately reflects colouration in wild birds. In this study, we use reflectance spectrometry to compare the plumage reflectance of avian museum skins and wild birds. We use long‐tailed manakins Chiroxiphia linearis, to investigate these potential differences in colour. Long‐tailed manakins are ideal for this type of study as their colourful plumage patches result from three primary plumage colouration mechanisms found in birds: melanin pigmentation, carotenoid pigmentation, and structural colouration. These features of their plumage allowed us to independently assess variation in each plumage colouration mechanism. Reflectance spectra obtained from museum specimens were very similar to those obtained from wild birds, and the colouration of specimens was usually well within the range of variation observed in wild birds. As such, museum specimens can accurately represent the colouration of wild birds. Nevertheless, we found significant differences in colouration between museum skins and wild birds. We documented differences in brightness, hue, saturation, and chroma, although the direction and magnitude of these differences varied by mechanism of colouration. Multivariate analyses revealed that the age of museum specimens and the time of year at which they were collected contributed to some of these differences. We discuss potential proximate causes of these changes in colour, many of which apply to both museum specimens and wild birds, and identify the types of studies that are likely to be most sensitive to these changes.

Predicting fate from early connectivity in a social network

In the long-tailed manakin (Chiroxiphia linearis), a long-lived tropical bird, early connectivity within a social network predicts male success an average of 4.8 years later. Long-tailed manakins have an unusual lek mating system in which pairs of unrelated males, at the top of complex overlapping teams of as many as 15 males, cooperate for obligate dual-male song and dance courtship displays. For as long as 8 years before forming stable "alpha-beta" partnerships, males interact with many other males in complex, temporally dynamic social networks. "Information centrality" is a network connectivity metric that accounts for indirect as well as shortest (geodesic) paths among interactors. The odds that males would rise socially rose by a factor of five for each one-unit increase in their early information centrality. Connectivity of males destined to rise did not change over time but increased in males that failed to rise socially. The results suggest that network connectivity is important for young males (ages 1-6) but less so for older males of high status (ages 10-15) and that it is difficult to explain present success without reference to social history.

Plumage Development and Molt in Long-Tailed Manakins (Chiroxiphia Linearis): Variation According to Sex and Age

AbstractLek-mating Long-tailed Manakins (Chiroxiphia linearis) exhibit an unusual pattern of delayed plumage maturation. Each year, males progress through a series of predefinitive plumages before attaining definitive plumage in their fifth calendar year. Females also exhibit variation in plumage coloration, with some females displaying male-like plumage characteristics. Using data from mist-net captures in northwest Costa Rica (n = 1,315) and museum specimens from throughout the range of Long-tailed Manakins (n = 585), we documented the plumage sequence progression of males, explored variation in female plumage, and described the timing of molt in this species. Males progressed through a series of age-specific predefinitive plumages, which enabled the accurate aging of predefinitive-plumaged males in the field; this predefinitive plumage sequence is the basis for age-related status-signaling in these males. Females tended to acquire red coloration in the crown as they aged. However, colorful plumage in females may be a byproduct of selection on bright male plumage. Females exhibited an early peak of molt activity from February to April, little molt from May through July, and a second, more pronounced peak of molt activity in October. By contrast, males in older predefinitive-plumage stages and males in definitive plumage exhibited comparable unimodal distributions in molt activity beginning in June and peaking between July and October. Our data are consistent with selective pressure to avoid the costs of molt-breeding overlap in females and older males. Our findings have important implications for social organization and signaling in Long- tailed Manakins, and for the evolution of delayed plumage maturation in birds.Desarrollo del Plumaje y Muda en Chiroxiphia linearis: Variación de Acuerdo al Sexo y la Edad

PLUMAGE DEVELOPMENT AND MOLT IN LONG-TAILED MANAKINS (CHIROXIPHIA LINEARIS): VARIATION ACCORDING TO SEX AND AGE

Lek-mating Long-tailed Manakins (Chiroxiphia linearis) exhibit an unusual pattern of delayed plumage maturation. Each year, males progress through a series of predefinitive plumages before attaining definitive plumage in their fifth calendar year. Females also exhibit variation in plumage coloration, with some females displaying male-like plumage characteristics. Using data from mist-net captures in northwest Costa Rica (n = 1,315) and museum specimens from throughout the range of Long-tailed Manakins (n = 585), we documented the plumage sequence progression of males, explored variation in female plumage, and described the timing of molt in this species. Males progressed through a series of age-specific predefinitive plumages, which enabled the accurate aging of predefinitive-plumaged males in the field; this predefinitive plumage sequence is the basis for age-related status-signaling in these males. Females tended to acquire red coloration in the crown as they aged. However, colorful plumage in females may be a byproduct of selection on bright male plumage. Females exhibited an early peak of molt activity from February to April, little molt from May through July, and a second, more pronounced peak of molt activity in October. By contrast, males in older predefinitive-plumage stages and males in definitive plumage exhibited comparable unimodal distributions in molt activity beginning in June and peaking between July and October. Our data are consistent with selective pressure to avoid the costs of molt-breeding overlap in females and older males. Our findings have important implications for social organization and signaling in Long- tailed Manakins, and for the evolution of delayed plumage maturation in birds. Desarrollo del Plumaje y Muda en Chiroxiphia linearis: Variación de Acuerdo al Sexo y la Edad

Ontogeny of sexual dimorphism in the Long‐tailed ManakinChiroxiphia linearis: long maturation of display trait morphology

Males of dimorphic species often show ornaments that are thought to have evolved through female choice or/and male–male competition. The sexual differentiation of similar morphologies occurs during ontogeny, resulting in differential sex and age‐specific selection. The Long‐tailed Manakin is a dimorphic species with a highly skewed mating system, the males of which delay plumage maturation over 3 to 4 years. We describe ontogenetic changes in feather morphology in this species through sexual maturity. Males showed a significant increase in length of the central rectrices with age, hence their degree of sexual dimorphism increased from zero in 1‐year‐old males to 189.5% in adults. In contrast, male tail length decreased with age. Wing length did not vary significantly with age, but females had relatively longer wings than males. Wing loading was greater in females and decreased with age in males. In adults, rectrix length was positively correlated with testis volume, supporting the hypothesis that secondary sexual characters can signal the condition of primary sexual characters. Rectrix length showed positive allometry with body size in males less than 4 years old, whereas older males showed negative allometry and females showed isometry. Wing area and wing loading shifted from negative to positive allometry in males of 2 to 3 years of age. Changes in male morphology during ontogeny in the Long‐tailed Manakin appeared to be associated with their specific display behaviours. Age‐related changes in allometric growth of rectrices in the Long‐tailed Manakin suggested that young males invest disproportionately more in the length of this trait relative to their body size. This investment could act as a signal of competitive ability to move status position in their orderly queue.

MICROSATELLITE DNA EVIDENCE FOR GENE FLOW IN NEOTROPICAL LEK-MATING LONG-TAILED MANAKINS

Abstract I genotyped lek-mating Long-tailed Manakins (Chiroxiphia linearis) at Monteverde and Santa Rosa, Costa Rica, 115 km apart. Cavalli-Sforza distance was 0.04, DLR was 0.18, and RST and θ were both 0.02. Bayesian clustering analysis indicated that both populations were part of a single cluster rather than from distinct clusters. I present a binomial test for probability of allelic absence as a function of sample size. Genotypic likelihood tests assigned 50% of Monteverde birds to Santa Rosa, versus 26% of Santa Rosa birds to Monteverde. Two lines of evidence supported the idea of asymmetric gene flow up the elevational gradient from Santa Rosa to Monteverde. Low differentiation at this spatial scale, despite intense sexual selection, suggests that sexual selection alone is unlikely to promote rapid divergence leading to speciation. Reduced gene flow, produced by geographic barriers or behavioral factors, may also be required. Evidencia de Flujo Genico Mediante ADN Microsatelital en Chiroxiphia linea...

The development of coordinated singing in cooperatively displaying long-tailed manakins

Long-tailed manakins (Chiroxiphia linearis) have a puzzling social system in which teams of two males display cooperatively in dispersed lek arenas, but only the alpha partner mates with visiting females. One benefit of performing as a nonmating partner might be to gain experience as an apprentice to improve the performance of the complex duet song and joint dance. We examined the relationship between the age of singers and two measures of singing performance: song variability and sound frequency matching. Singing performance improved with age; variability in four song characteristics of males less than 3 years old was greater than that in their older partners, and frequency matching increased with the age of the younger partner. Randomization tests of song samples from seven well-established teams showed that males did not track the song-to-song variation in their partners' singing. Another randomization test showed that frequency matching by these teams was higher than that of randomly paired partners. We considered three alternative hypotheses for the congruent songs: (1) short-term accommodation to the partner's song; (2) active choice of partners with similar intrinsic frequencies; and (3) long-term development of congruent song through either practice or song copying. Our results and evidence from long-term monitoring of banded birds best support the hypothesis that frequency matching develops over several years during the complex and protracted process of partner formation. Nonmating males may benefit from increasing their competence at display, eventually enjoying increased mating success when they inherit display sites from older males. Copyright 2002.

Uniformity of Long-tailed Manakin Songs from Three Localities in Costa Rica

Microgeographic variation in song is a well-documented consequence of song learning in many songbirds, but the relationship between song variation and development in the suboscines is poorly understood. Because learning appears to play a role in song development in Long-tailed Manakins (Chiroxiphia linearis), we wanted to find out whether they also exhibit microgeographic variation in song. We compared songs of Long-tailed Manakins from three localities in Costa Rica using multivariate analysis of variance and canonical discriminant analysis of five song variables. Differences among localities were not significant, and songs from the same localities did not cluster together in a canonical plot. This finding is similar to those observed in suboscine flycatchers whose songs are innate.