Testosterone and its effects on courtship in golden-collared manakins (Manacus vitellinus): seasonal, sex, and age differences

Male golden-collared manakins gather on leks and perform an acrobatic display to attract females. In temperate breeding species, testosterone (T) activation of courtship displays has been well studied. Few studies have examined T activation of displays in tropical species; even fewer have explored the activational role of T in elaborate courtship displays such as in the manakin. In some tropical species, including manakins, territorial aggression or song behavior are uncoupled from T. We have previously shown that T activates display behavior in manakin males when endogenous T levels are low in the non-courtship season. To understand how T functions in breeding birds, we examined T levels in a large group of manakins sampled during the courtship and non-courtship season. In addition, during the courtship season, we gave T implants to adult males, juvenile males, and females. We found that T levels were low during the non-courtship season and comparatively higher on average during the courtship season. However, T levels were low in many adult males during the courtship season, especially when compared to temperate breeding species. Regardless of initial endogenous T levels during the courtship season, T implants did not increase the display frequency of adult males. T-treated females and juvenile males did display under similar conditions. Our data suggest that the effects of T on manakin display vary with season, sex, and age and that high T is not necessary for display.     

High-Speed Video Analysis Reveals Individual Variability in the Courtship Displays of Male Golden-Collared Manakins

The males of the Golden-collared manakin ( Manacus vitellinus ), a passerine bird of the Neotropical region, perform elaborate courtship displays that are among the most spectacular in the animal kingdom. During a 7-mo long breeding season, male manakins aggregate in leks of up to 12 individuals, and each male clears a small 'court' on the forest floor where he spends several hours per day performing his displays either with or without the presence of a female. Like males of other manakin species, males of M. vitellinus produce loud mechanical sounds with their wings during the displays. The elaborate displays of the manakins are thought to be the result of sexual selection, which is particularly intense in lekking species in which females choose their mate mainly on the basis of behavioural and morphological features. However, we know little about differences in display between male manakins which may be related to individual differences in reproductive success. A quantitative, detailed analysis of the courtship displays has been difficult because the birds' movements are too fast to be studied with standard video recording techniques. For the first time, we recorded the displays of male Golden-collared manakins in the forest of Panama with a high-speed camera that allows a time resolution 5–40 times higher than that of a standard video camera. We found that several elements of the displays differed significantly between individuals. In addition, the slow-motion analysis revealed the features of the displays that had not been described in previous studies. Individually different features of the displays may form the basis for female choice and will allow testing hypotheses about the evolution of the manakin displays by sexual selection and their importance for speciation mechanisms in the genus Manacus .     

Androgen and the elaborate courtship behavior of a tropical lekking bird

In most bird species, male courtship behavior is controlled by testosterone (T) and its metabolites. In species breeding in temperate and arctic regions T circulates at high levels during a relatively short courtship period because high levels of T can be costly in terms of immunocompetence and parental care. Few studies have investigated androgen modulation of courtship behavior in tropical birds. Male golden-collared manakins (Manacus vitellinus) aggregate in leks for several months and perform spectacular, acrobatic courtship displays. Here we examined whether T is elevated in golden-collared manakins during the displaying period and if courtship behavior is modulated by androgen action on androgen receptors. We measured T levels in displaying males at the beginning of the breeding season and again, one month later. In addition, both wild and captive males were treated with the anti-androgen, flutamide, and their courtship behavior was recorded for several weeks. T levels were relatively high shortly after leks were established but decreased substantially a month later, even though the amount of courtship did not change. Flutamide reduced male courtship activity for one week, but display behavior then increased after two weeks of flutamide treatment. Our studies show that androgens modulate male manakin courtship, but the amount of courtship is not directly correlated with the concentration of circulating T. These results suggest that the relationships between androgen and courtship might differ between tropical and temperate birds.     

Neuromuscular and endocrine control of an avian courtship behavior

In many species of birds, males perform complex visual and acoustic courtship displays to attract and stimulate females. Some of these displays involve considerable use of the wings and legs, suggesting that they may be controlled by sexually dimorphic spinal motoneurons and their target muscles. Sex steroid hormones are known to organize and activate many sexually dimorphic phenotypes, so these neuromuscular systems may also be steroid sensitive. To test these ideas, we have begun studies of wild golden-collared manakins (Manacus vitellinus) in Central America. Males of this species establish a courtship arena in the forest, where they perform an elaborate dance that includes use of their wings to generate loud snapping sounds. Here we describe male golden-collared manakin courtship behavior, including the various "wingsnaps." We also review our studies, and those of others, showing sexually dimorphic properties of manakin wings, the wing musculature, and sex steroid accumulation in the spinal cord. These data suggest that manakins are useful models for evaluating steroid control of complex peripheral neuromuscular systems.     

Hormonal correlates of social status and courtship display in the cooperatively lekking lance-tailed manakin

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations.     

Males in seemingly female‐like plumage do not mimic females: UV reflectance reveals temporal cryptic dimorphism in a manakin species exhibiting delayed plumage maturation

Manakins (Pipridae) are neotropical birds that usually exhibit delayed plumage maturation (DPM). Thus, while plumage of most adult male manakins is brightly conspicuous, subadult males and females are basically dull‐olive green. Although sexual dichromatism in some bird species may be evident only through UV reflectance, this phenomenon, known as hidden sexual dichromatism, has not been previously studied in manakins to compare subadult males and females. Within this framework, we carried out spectrophotometric analyses in searching for hidden sexual dichromatism in the white‐bearded manakin Manacus manacus, through comparison of UV spectra in females and subadult males in green plumage. Our results revealed UV reflectance in both sexes in green plumage. Moreover, we found UV spectral differences in homologous color patches between sexes, particularly at belly. Since the observed differences may allow intraspecific sex recognition of individuals in green plumage, our results do not support the female‐mimicry hypothesis to explain delayed plumage maturation in the white‐bearded manakin. Although our findings dismiss the female mimicry hypothesis, we cannot state whether these results support the non‐mutually exclusive cryptic and status signaling hypotheses. We propose then, that dull coloration of subadult males may serve both as a cryptic trait and to limit the energetic costs of acquiring the adult plumage before sexual maturity. Meanwhile, differential UV color traits between sexes in green plumage may allow adult males to avoid unnecessary energy expenditures in courtship displays in the presence of males near leks, and to selectively focus their the courtship displays on females. In accordance with the status signaling hypothesis, subadult males can be recognized both as males and subordinates and consequently may practice courtship displays without suffering aggressions by adult males. Our results highlight the importance to include a wider range of spectrophotometric information analyses for testing hypotheses regarding delayed plumage maturation.     

Microsatellite DNA analysis shows that greater sage grouse leks are not kin groups

The spectacular social courtship displays of lekking birds are thought to evolve via sexual selection, but this view does not easily explain the participation of many males that apparently fail to mate. One of several proposed solutions to this 'lek skew paradox' is that kin selection favours low-ranking males joining leks to increase the fitness of closely related breeders. We investigated the potential for kin selection to operate in leks of the greater sage grouse, Centrocercus urophasianus, by estimating relatedness between lekking males using microsatellite DNA markers. We also calibrated these estimates using data from known families. Mean relatedness within leks was statistically indistinguishable from zero. We also found no evidence for local clustering of kin during lek display, although males tended to range closer to kin when off the lek. These results make kin selection an unlikely solution to the lek skew paradox in sage grouse. Together with other recent studies, they also raise the question of why kin selection apparently promotes social courtship in some lekking species, but not in others.     

Massive, solidified bone in the wing of a volant courting bird

One pervasive morphological feature of tetrapods is the pipe-like, often marrow-filled, structure of the limb or long bones. This 'hollow' form maximizes flexural strength and stiffness with the minimum amount of bony material, and is exemplified by truly hollow (air-filled), or pneumatic, humeri in many modern birds. High-resolution microCT scans of the wings of two male club-winged manakins (Machaeropterus deliciosus) uncovered a notable exception to the hollow-tube rule in terrestrial vertebrates; males exhibited solidified ulnae more than three times the volume of birds of comparable body size, with significantly higher tissue mineral densities. The humeri exhibited similar (but less extreme) modifications. Each of the observed osteological modifications increases the overall mass of the bone, running counter to pervasive weight-reducing optimizations for flight in birds. The club-winged manakin is named for a pair of unique wing feathers found in adult males; these enlarged feathers attach directly to the ulna and resonate to produce a distinctive sound used in courtship displays. Given that the observed modifications probably assist in sound production, the club-winged manakin represents a case in which sexual selection by female choice has generated an ecologically 'costly' forelimb morphology, unique in being specialized for sound production at a presumed cost in flight efficiency.     

Female choice for male motor skills

Sexual selection was proposed by Darwin to explain the evolution of male sexual traits such as ornaments and elaborate courtship displays. Empirical and theoretical studies have traditionally focused on ornaments; the reasons for the evolution of elaborate, acrobatic courtship displays remain unclear. We addressed the hypothesis that females choose males on the basis of subtle differences in display performance, indicating motor skills that facilitate survival. Male golden-collared manakins (Manacus vitellinus) perform elaborate, acrobatic courtship displays. We used high-speed cameras to record the displays of wild males and analysed them in relation to male reproductive success. Females preferred males that performed specific display moves at greater speed, with differences of tens of milliseconds strongly impacting female preference. In additional males, we recorded telemetrically the heart rate during courtship using miniature transmitters and found that courtship is associated with profoundly elevated heart rates, revealing a large metabolic investment. Our study provides evidence that females choose their mates on the basis of subtle differences in motor performance during courtship. We propose that elaborate, acrobatic courtship dances evolve because they reflect motor skills and cardiovascular function of males.     

Loss of sexual dimorphism is associated with loss of lekking behavior in the green manakin Xenopipo holochora

Manakins (Pipridae) are well know for elaborate male sexual displays and ornate plumage coloration, both of which are thought to have evolved as a consequence of lekking breeding, the prevalent mating system in the family. Less attention has been paid to a handful of ‘drab’ manakin species, in which sexual dimorphism appears to be reduced or absent. Using character reconstruction, we show that these ‘exceptions to the rule’ represent phylogenetically independent cases of losses in sexual dimorphism, and as such could provide a focal group to investigate the link between changes in morphology and in life history (e.g. mating system). We take a first step in this direction by focusing on two subspecies of the putatively monomorphic green manakin Xenopipo holochlora to formally confirm that the species is sexually monomorphic in size and plumage color and test the prediction that sexual monomorphism is associated with the loss of lekking behavior in this species. Our results show that size dimorphism is present but limited in the green manakin, with substantial overlap in male and female morphometric measures, and that sexes are largely monochromatic (including from an avian perspective), despite marked coloration differences between subspecies. Behavioral observations indicate that males do not form leks and do not engage in elaborate sexual displays, that there is no stable pair bond formation, and that females provide parental care alone. These findings are consistent with the idea that changes in mating behavior may have driven changes in morphology in Pipridae, and we encourage similar studies on other drab manakins to better understand this relationship.     

Plumage brightness predicts male mating success in the lekking golden-collared manakin, Manacus vitellinus

The evolution of colorful plumage has been dramatic in lekkingspecies. Several studies show that the size of colorful traitsinfluence female choice in leks; however, relatively littleis known about the specific function of color, in particularits spectral properties, in lekking taxa. To determine the importanceof color in a lekking species, we monitored the mating successof male golden-collared manakins, Manacus vitellinus, and relatedthis to spectral measures of their colorful plumage, as wellas other morphological and behavioral traits shown to be importantin other lekking species. We found that lek centrality, malebody size, and plumage brightness were associated with malemating success. Only plumage brightness, however, entered amultiple regression model, indicating that plumage is the overallbest predictor of mating success. These results provide evidencethat the spectral properties of colorful plumage predict malemating success in a lekking species and provide important insightinto why many lekking birds are dichromatic and elaborate incoloration.     

Assessing lek attendance of male greater sage-grouse using fine-resolution GPS data: Implications for population monitoring of lek mating grouse

Counts of males displaying on breeding grounds are the primary management tool used to assess population trends in lekking grouse species. Despite the importance of male lek attendance (i.e., proportion of males on leks available for detection) influencing lek counts, patterns of within season and between season variability in attendance rates are not well understood. We used high-frequency global positioning system (GPS) telemetry data from male greater sage-grouse (Centrocercus urophasianus; n = 67) over five lekking seasons (2013–2017) at eight study sites in Nevada to estimate lek attendance rates. Specifically, we recorded daily locations of sage-grouse in relation to mapped lek boundaries and used generalized additive models to assess temporal variation in attendance rates by age class (subadult vs. adult). Average timing of peak attendance occurred on 16 April but varied from March 16, 2014 to April 21 , 2016. Overall, adult males attended leks at higher rates (0.683 at peak) and earlier in the season (19 March) than subadults (0.421 at peak on April 19). Peak attendance probability was positively related to cumulative winter precipitation. Daily probabilities of lek switching differed between adults (0.019 at peak on March 3) and subadults (0.046 at peak on March 22), and lek switching was negatively related to distance to nearest lek. Our results indicate variable patterns in lek attendance through time, and that lek switching may occur at higher rates than previously thought. We demonstrate the use of generalizable daily attendance curves to date-correct lek counts and derive estimates of male abundance, although such an approach will likely require the incorporation of information on age structure to produce robust results that are useful for population monitoring.     

Sharp-tailed grouse lek attendance and fidelity in upper Michigan

To assess and improve existing monitoring protocols for sharp-tailed grouse (Tympanuchus phasianellus) in the eastern Upper Peninsula of Michigan, we used data from 58 radio-collared grouse (46 M, 12 F) monitored within 3 openland landscape types: a xeric, conifer-dominated site, a wetland-dominated site, and a site dominated by low-intensity agriculture. We used lek counts and radio telemetry to determine lek attendance rates, factors affecting lek attendance rates, lek fidelity, and inter-sexual variation in these parameters. Our analysis indicated lek attendance varied with respect to sex of bird, day of year, time after sunrise, and wind speed. Peak male lek attendance rates exceeded those of females by up to 40%, and peak lekking activity for both males and females occurred during the second and third weeks of April. Male lekking activity occurred earlier and was sustained longer than that of females. Lekking activity was negatively related to time of day and wind speed. We observed strong lek fidelity as radio-collared birds attended a primary lek 94% of the time, indicating a low probability of multiple counting of individual birds. We also proposed a method to adjust lek count data for the probability that birds are on a lek during lek counts. Our proposed method can be used by researchers and managers to improve estimates of the number of birds attending a lek by reducing the negative bias associated with observed counts. © 2011 The Wildlife Society.     

Trade-offs between activity and thermoregulation in a small carnivore,the least weasel Mustela nivalis

We studied factors influencing daily energy expenditures (DEE) of male least weasels (Mustela nivalis) using the doubly labelled water technique. The relationship between ambient temperature and DEE formed a triangular pattern, characterized by invariance of the maximum DEE and an inverse relationship between minimum DEE and temperature. A simple energetic model relating the DEE of male weasels to activity time (AT) and ambient temperature predicted that, across seasons, less than 10 per cent of measurements approach the upper bound of observed DEE. Male weasels were able to maintain a relatively constant maximum energy output across varying temperatures by adjusting their AT to changes in temperature. They achieved maximum energy expenditures in winter due to high thermoregulatory costs, and in spring and summer due to high levels of physical activity. This pattern exemplifies a ‘metabolic niche’ of a small mammal having extremely high energy expenditures primarily driven by ambient temperature.     

Seasonal sex–specific energy expenditure in breeding and non-breeding Palestine sunbirds Nectarinia osea

The timing of the chick‐rearing phase is known to have a profound effect on the reproductive success of birds. However, little is known about the energetic costs faced by the parents during different periods of the breeding season. These costs may have vital consequences for both their survival and future reproduction. In most studies, daily energy expenditure (DEE) of breeding and non‐breeding birds has been compared, without controlling for the effect of season. In the present study, we examined the energy demands of breeding compared to non‐breeding Palestine sunbirds Nectarinia osea and whether there were sex‐specific differences in DEE within and between different seasons. We predicted that DEE would be elevated when birds rear chicks, especially at cooler ambient temperatures. Time‐energy budgets were constructed for pairs of sunbirds, rearing chicks, or not breeding, in spring and summer. There were significant seasonal differences in estimates of DEE in non‐breeders that were 21% higher in spring than in summer. We attributed these to increases in non‐flight metabolic rate rather than changes in time spent on different activities. Our estimates of DEE for the birds that were rearing chicks were higher than non‐breeding adults. In females the increase in DEE when breeding, compared to when not breeding, was similar in both spring and summer, while males increased their DEE much less when breeding in spring. The differences in estimated DEE, however, were not significant between male and female birds in any season. Between seasons, female breeders had 17.1% higher DEE in spring than in summer, while male breeders showed no difference in DEE when rearing chicks in different seasons. Accordingly, our initial prediction was supported, as DEE in chick‐rearing adults was higher than in non‐breeding adults. In addition, although temperatures are lower in spring, breeding in the spring is only more costly than breeding in summer for females. Apparently, males are more flexible in reallocating their time and energy spent on different activities.     

Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks

1. The objective of the work reported here was to test the hypothesis that in insects that invest considerable energy in sexual displays and courtship, foraging successfully for food affects their subsequent performance and copulatory success in leks. Accordingly, the interactions between body size and diet on initiation of lekking behaviour and copulatory success in male Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) were investigated. 2. Protein‐fed males were heavier and contained more protein and less lipid reserves than protein‐deprived males. Protein‐fed males were more likely to emit pheromone in leks and, consequently, were more likely to copulate than protein‐deprived males. Furthermore, protein‐fed males tended to start calling earlier than their nutritionally deprived competitors. 3. Though size was not related to initiation of lek behaviour, large males were more likely to copulate than small males. Among protein‐fed males, large individuals tended to mate earlier than smaller individuals. 4. Generally, in lek mating systems where a considerable investment of time and energy is required by males, foraging successfully for nutritional resources prior to engaging in territorial or courtship behaviour is essential for reproductive success.     

动物求偶场交配制度及其发生机制

求偶场是动物在繁殖期的集群求偶交配的场所, 是动物求偶与繁殖行为的表达空间。为探索求偶场的发生及其进化机制, 研究者们在短短20 年中提出了近10 种关于求偶场发生与进化机制的假说与模型。在鸟类、哺乳类、两栖爬行类和鱼类中已广泛地展开有关求偶场的研究, 但目前国内却还鲜见相关研究报道。本文介绍了求偶场的特征、类型及其进化假说与模型。结合保护生物学理论, 简单阐述了求偶场研究的保护生物学及行为生态学意义。     

Correlates of male mating success in a lekking bird with male-male cooperation

Correlates of male mating success were examined in a population of long-tailed manakins, Chiroxiphia linearis, that included 270 colour-banded individuals. Long-tailed manakins have a lek mating system and male-male cooperation in courtship display. Multivariate analysis of behavioural variables indicated that female visitation correlated with the number of unison ‘toledo’ calls given by male partners. Given a female vist, copulatory success was correlated with the ‘butterfly’ display component of the dual-male dance. Both ‘toledo’ output and dance display differed significantly between perch-zones. Only six to eight partnerships in a local population of as many as 55 males per season performed call displays at a level (75–335 toledos per h) that was correlated with any female visitation. Data on crown plumage of female visitors suggested that younger females may have been less discriminating than were older females. The relationship between variance in mating success and the evolution of cooperative male display is discussed.     

Adaptations for avian frugivory: assimilation efficiency and gut transit time of Manacus vitellinus and Pipra mentalis

Summary I examined the digestive physiology of two avian frugivores, the golden-collared manakin, Manacus vitellinus, and the red-capped manakin, Pipra mentalis, to discover how these birds extract energy from fruit. Using 14 species of fruit in the natural diet of manakins, I examined the assimilation of nutrients from fruit pulp, fruit passage rates, seed passage rates, and gut morphology. Fruits in the manakins' diets had high water content (average, 84%) and low nutrient concentrations (3 kJ/g wet pulp; 17 kJ/g dry pulp; 1% nitrogen/g dry pulp). Manacus and Pipra did not differ in the average assimilation of energy in fruit pulp (63%), although it varied from 37 to 84% depending on fruit species. Assimilation of total nonstructural carbohydrates in the fruit pulp was very high (86–98%) in both species. Gut evacuation was rapid; maximum transit time of a labeled fruit was 30 min. Seeds passed through the gut faster (Manacus: 15 min; Pipra: 12 min) than the accompanying fruit epidermis (both spp: 22 min). Manakins regurgitated large seeds (>5 mm diameter) in 7 to 9 min. Rapid gut passage time, high assimilation of nonstructural carbohydrates, and the selective regurgitation and rapid elimination of bulky seeds enable manakins to process a large volume of food per day. By increasing rates of fruit intake and gut passage, manakins can effectively increase total nutrient uptake. These adaptations of manakins are requisite for harvesting sufficient nutrients from fruit, due to its low nutrient density, high water content, and bulky seeds.