Inferring performance in the songs of dark-eyed juncos (Junco hyemalis)

Within bird species, songs differ in their attractiveness tofemales or effectiveness in male–male interactions. Somesongs are more difficult to sing than others, and receiversmay use a singer's performance of difficult songs as a meansfor evaluating the quality of the singer. The concept of songperformance aims at quantifying how physiologically demandingare different songs. Using variation between song types of dark-eyedjuncos, Junco hyemalis, we show that some song traits tradeoff with costly aspects of song output—short intervalsbetween syllables or loud sound amplitude—suggesting thatthose traits are difficult to sing. First, after controllingfor other traits, long syllables require longer intervals forrecovery. This supports the idea that a measure of "respiratoryperformance" could be based on the relative lengths of syllablesand intervals. Second, some syllable traits trade off stronglywith sound amplitude, suggesting that these traits may be difficultto sing at high amplitudes. The ratio of frequency bandwidthand trill rate has been used to infer performance in other birdspecies, but we found no evidence that frequency bandwidth tradesoff with any aspect of song output in the junco. The negativeassociation of bandwidth with trill rate may instead be a passiveconsequence of syllable length, with longer syllables randomlyaccumulating frequency modulation. We conclude that bird receiversmay best evaluate how well a song is performed if they integratemultiple cues and discuss how researchers may similarly devisemeasures of song performance.     

Photoperiod and testosterone independently affect vocal control region volumes in adolescent male songbirds

Previously, we found that, unlike adults, adolescent male dark-eyed juncos (Junco hyemalis) maintained large Area X volumes despite having low plasma testosterone concentrations. Other studies indicate that photoperiod may act independently of testosterone to modulate vocal control region (VCR) volumes in adult songbirds. In the present study, we investigated the effects of testosterone and photoperiod on the volumes of four VCRs in adolescent male juncos. To test the hypothesis that VCR volumes in these males are testosterone independent, we treated birds exposed to short days with testosterone and later compared their VCR volumes with those of birds exposed to short days without testosterone. To examine whether photoperiod alone could affect VCR volumes independent of testosterone, we measured these volumes in photorefractory birds exposed to long photoperiod without testosterone. Administering testosterone induced singing, yet increased the volume of only one VCR, the robust nucleus of the anterior neostriatum (RA). In contrast, long photoperiod increased several VCR volumes (Area X, higher vocal center, and RA) despite low testosterone levels, but did not induce singing. Our results suggest a limited role for testosterone, but an important role for photoperiod, in controlling VCR volumes in adolescent male juncos. In addition, the results demonstrate that singing behavior can be induced in adolescent males without a concomitant increase in most VCR volumes. © 1998 John Wiley & Sons, Inc. J Neurobiol 36: 550–558, 1998     

Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis)

In male dark-eyed juncos (Junco hyemalis), experimentally elevated testosterone (T) decreases male parental care and offspring survival, but results in higher overall fitness through greater mating success. To help address the ensuing question of what prevents selection from favoring higher levels of T in male juncos, we manipulated T in female juncos. A previous study demonstrated no effect of experimentally elevated T on female incubation behavior, suggesting that female parental behavior might be insensitive to T. In this study we asked whether experimentally elevated T mediates other female parental behaviors and whether variation in T-mediated parental behavior might influence reproductive success. We videotaped free-living control- and T-females during nesting to quantify brooding behavior when young were 3 days old and provisioning behavior when young were 6 days old. Nest defense was measured by quantifying responses to a mounted predator placed near the nest. Reproductive success was assessed via fecundity, nestling quality, and nest survival. T-females spent less time than control females brooding but did not differ in provisioning rate. T-females performed fewer dives at the predator mount and, unlike controls, failed to increase defense as nesting progressed. T-females also had lower daily nest survival and lower nest success (odds of producing at least one fledgling). We conclude that some aspects of female parental behavior are sensitive to experimentally elevated T while others are not and consider the implications for the evolution of T-mediated characters in both sexes.     

Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis)

In seasonally breeding male oscines, song learning and expression are controlled by brain regions (vocal control regions, VCRs) that exhibit seasonal neural plasticity in adulthood. Several VCRs contain androgen receptors, and gonadal androgens play important roles in the control of seasonal structural and functional changes of VCRs. Recent studies also found that adult VCRs are influenced by factors other than gonadal hormones, including photoperiod, but the relative importance of these factors and their mechanisms of action are poorly understood. To address this issue, we investigated the contributions of photoperiod and testicular androgens to the regulation of VCR volumes and to the control of song expression in adult dark-eyed juncos, Junco hyemalis. Exposing castrated (CX) photosensitive males to long days (LD) enhanced their high vocal center (HVc) volumes compared to those of males held on short days (SD). These volumes were not further increased by concurrent testosterone (T) treatment, revealing a marked and gonadal androgen-independent stimulatory influence of photoperiod on the size of this brain region. HVc sizes were smaller in LD-exposed photorefractory than photosensitive males irrespective of whether birds were intact or had been castrated before photoperiodic manipulations, but HVc sizes increased in response to T treatment in intact photorefractory males. Thus, LD exposure can increase HVc volumes in the absence of gonadal T, but large volume induction in photorefractory males requires elevated plasma T levels. Testosterone treatment of SD-exposed photosensitive males increased HVc, but not Area X, MAN, or RA volumes. Only T-treated males sang and this treatment given to castrates was equally effective behaviorally when administered to photosensitive, photostimulated, or photorefractory juncos. This result indicates that the stimulating influence of LD exposure on HVc volumes is insufficient to induce song in the absence of elevated plasma T levels.     

Wing and leg bone microstructure reflects migratory demands in resident and migrant populations of the Dark-eyed Junco (Junco hyemalis)

Migration is the primary strategy that temperate birds use to avoid overwintering under harsh conditions. As a consequence, migratory birds have evolved specific morphological features in their wings and skeleton. However, in addition to varying in overall shape and size, bone can also change at the microstructural level by, for example, increasing its thickness. Such changes are critical to preventing fracture and damage under repeated loading (fatigue), yet it is not known whether migratory behaviour influences bone microstructure. To address this gap in the literature, we performed micro-computed tomography on skeletons of resident and migrant subspecies of the Dark-eyed Junco Junco hyemalis. We investigated the differences in the major wing bone, the humerus, and the major leg bone, the femur. In each bone, we studied the microarchitecture of the two types of bone tissue: cortical bone, the thick outer layer of bone; and trabecular bone, which is the porous network of bone tissue at the ends of long bones. We used linear models to quantify morphological features with respect to body mass and migratory behaviour. Humeri from migratory birds were thinner, wider and had higher overall geometric stiffness, i.e. a higher polar moment of inertia, relative to humeri from resident birds. These features may help keep their bones stiff to maintain their increased body mass during migration. In contrast, migrant femora were shorter, thinner and had lower geometric stiffness than femora of residents, potentially to reduce total body mass. Tissue mineral density was lower in both the humerus and the femur of migratory birds. In addition, migratory subspecies had less trabecular bone (lower bone volume fraction) due primarily to a loss of trabecular thickness. Migratory behaviour may thus select for improved stiffness and fatigue resistance in the wing bones and reduced mass of leg bones. Our work demonstrates how important insights into morphological adaptation can be obtained by investigating bone microstructure.     

Maturation‐dependent control of vocal temporal plasticity in a songbird

Birdsong is a unique model to address learning mechanisms of the timing control of sequential behaviors, with characteristic temporal structures consisting of serial sequences of brief vocal elements (syllables) and silent intervals (gaps). Understanding the neural mechanisms for plasticity of such sequential behavior should be aided by characterization of its developmental changes. Here, we assessed the level of acute vocal plasticity between young and adult Bengalese finches, and also quantified developmental change in variability of temporal structure. Acute plasticity was tested by delivering aversive noise bursts contingent on duration of a target gap, such that birds could avoid the noise by modifying their song. We found that temporal variability of song features decreased with birds' maturation. Noise‐avoidance experiments demonstrated that maximal changes of gap durations were larger in young that in adult birds. After these young birds matured, the maximal change decreased to a similar level as adults. The variability of these target gaps also decreased as the birds matured. Such parallel changes suggest that the level of acute temporal plasticity could be predicted from ongoing temporal variability. Further, we found that young birds gradually began to stop their song at the target gap and restart from the introductory part of song, whereas adults did not. According to a synaptic chain model for timing sequence generation in premotor nuclei, adult learning would be interpreted as adaptive changes in conduction delays between chain‐to‐chain connections, whereas the learning of young birds could mainly depend on changes of the connections. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 995–1006, 2017     

Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis)

This study investigates the effects of captivity and testosterone treatment on the volumes of brain regions involved in processing visual and spatial information in adult dark-eyed juncos (Junco hyemalis). We treated captive and free-living male juncos with either testosterone-filled or empty implants. Captive juncos had a smaller hippocampal formation (HF) (both in absolute volume and relative to telencephalon) than free-living birds, regardless of hormone treatment. Testosterone-treated males (both captive and free-living) had a smaller telencephalon and nucleus rotundus, but not a smaller HF or ectostriatum, than controls. We found that free-living testosterone-treated males had larger home ranges than free-living controls in agreement with earlier experiments, but we found no corresponding difference in HF volume. We discuss the implications of the effect of captivity on HF volume for past and future laboratory experiments.     

Effects of captivity and testosterone on the volumes of four brain regions in the dark‐eyed junco (Junco hyemalis)

This study investigates the effects of captivity and testosterone treatment on the volumes of brain regions involved in processing visual and spatial information in adult dark‐eyed juncos (Junco hyemalis). We treated captive and free‐living male juncos with either testosterone‐filled or empty implants. Captive juncos had a smaller hippocampal formation (HF) (both in absolute volume and relative to telencephalon) than free‐living birds, regardless of hormone treatment. Testosterone‐treated males (both captive and free‐living) had a smaller telencephalon and nucleus rotundus, but not a smaller HF or ectostriatum, than controls. We found that free‐living testosterone‐treated males had larger home ranges than free‐living controls in agreement with earlier experiments, but we found no corresponding difference in HF volume. We discuss the implications of the effect of captivity on HF volume for past and future laboratory experiments. © 2000 John Wiley & Sons, Inc. J Neurobiol 43: 244–253, 2000     

Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird

In many species, male territorial aggression is tightly coupled with gonadal secretion of testosterone (T). In contrast, in song sparrows (Melospiza melodia morphna), males are highly aggressive during the breeding (spring) and nonbreeding (autumn and early winter) seasons, but not during molt (late summer). In aggressive nonbreeding song sparrows, plasma T levels are basal (< or = 0.10 ng/ml), and castration has no effect on aggression. However, aromatase inhibitors reduce nonbreeding aggression, indicating a role for estrogen in wintering males. In the nonbreeding season, the substrate for brain aromatase is unclear, because plasma T and androstenedione levels are basal. Aromatizable androgen may be derived from plasma dehydroepiandrosterone (DHEA), an androgen precursor. DHEA circulates at elevated levels in wintering males (approximately 0.8 ng/ml) and might be locally converted to T in the brain. Moreover, plasma DHEA is reduced during molt, as is aggression. Here, we experimentally increased DHEA in wild nonbreeding male song sparrows and examined territorial behaviors (e.g., singing) and discrete neural regions controlling the production of song. A physiological dose of DHEA for 15 days increased singing in response to simulated territorial intrusions. In addition, DHEA treatment increased the volume of a telencephalic brain region (the HVc) controlling song, indicating that DHEA can have large-scale neuroanatomical effects in adult animals. The DHEA treatment also caused a slight increase in plasma T. Exogenous DHEA may have been metabolized to sex steroids within the brain to exert these behavioral and neural effects, and it is also possible that peripheral metabolism contributed to these effects. These are the first results to suggest that exogenous DHEA increases male-male aggression and the size of an entire brain region in adults. The data are consistent with the hypothesis that DHEA regulates territorial behavior, especially in the nonbreeding season, when plasma T is basal.     

Potential age differences in the migratory behaviour of a nocturnal songbird migrant during autumn and spring

In migratory songbirds, older individuals are thought to be more efficient migrants than younger individuals. Age‐specific differences in migratory efficiency have been reported mainly in respect of arrival timing, energy stores, rate of energy accumulation, departure behaviour, and departure direction. Yet, these traits were rarely assessed simultaneously in a single species. We further lack information whether age‐specific differences in behavioural traits present in autumn still manifest to the same degree in spring. Here we used the northern wheatear Oenanthe oenanthe, a long‐distance nocturnal songbird migrant, and investigated age‐specific differences in energy stores at capture (autumn: 1059 birds/spring: 803 birds), rate of energy accumulation (168/147), nocturnal departure timing (126/105), and departure direction (94/77) for both seasons. We found that in autumn, young northern wheatears departed significantly later in the night than older birds. This difference was not observed in spring. The resulting advance in nocturnal departure timing by young birds from autumn to spring may be due to learning based on experience gained during autumn, and/or to selective disappearance of those young individuals showing late departure times during autumn. We found no age‐specific difference in any of the other migratory traits investigated. To get a better understanding of age effects in songbird migrants, we need to study the potential adjustments of migratory behaviour within the individual over its life time. By individually tracking songbirds throughout their lifetime, we could start estimating whether a certain migratory decision (fuelling, departure, orientation) translates into higher (or lower) fitness, and whether individuals adjust their migratory behaviour based on learning from ‘wrong decisions’.     

Context matters: female aggression and testosterone in a year-round territorial neotropical songbird (Thryothorus leucotis)

Testosterone promotes aggressive behaviour in male vertebrates during the breeding season, but the importance of testosterone in female aggression remains unclear. Testosterone has both beneficial and detrimental effects on behaviour and physiology, prompting the hypothesis that selection favours an association between aggression and testosterone only in certain contexts in which intense or persistent aggression may be beneficial. We tested this hypothesis in a year-round territorial female buff-breasted wrens (Thryothorus leucotis), by exposing free-living females to experimental intrusions in different social (either single female or male, or paired decoys) and seasonal (pre-breeding or breeding) contexts. Females responded more aggressively to intrusions by females and pairs than to males. However, female intrusions elicited stronger responses during pre-breeding, whereas responses to pair intrusions were more intense during breeding. Territorial females had elevated testosterone levels after female intrusions and intermediate levels after pair intrusions during pre-breeding, but the levels of testosterone remained low after these intrusions during breeding. These results demonstrate seasonal differences in circulating testosterone following territorial aggression in female buff-breasted wrens and are suggestive of differences according to social context as well. Context-dependent elevation of testosterone implies that selection acts directly on female vertebrates to shape patterns of testosterone secretion.     

Seasonality of LH,testosterone and sperm parameters in spider monkey males (Ateles geoffroyi)

There are no reported data on hormonal fluctuations in black‐handed spider monkey males. On previous research about the reproductive physiology of this monkey we have found that during the dry season females show ovulatory estrogen peaks and males present the best quality semen. As part of an ongoing research, in this study we assessed seasonal variations in the concentration of serum luteinizing hormone (LH) and testosterone (T) in three adult spider monkey males to corroborate the seasonal reproductive synchrony. At the same time sperm count and motility were evaluated to search for any correlation between those sperm parameters and hormonal concentrations. We took blood and semen samples (by electroejaculation) of anesthetized males throughout the rainy (June–September) and dry (October–May) months. Our results revealed that T and LH were higher throughout the dry season and there was a significant correlation between T concentration and sperm count. Although higher during the dry season, sperm motility tended to correlate with testosterone and LH levels. These results demonstrated that black‐handed spider monkeys have a tendency to show a seasonal pattern of reproduction being the dry season the most likely time to achieve fertilization. Am. J. Primatol. 71:427–431, 2009. © 2009 Wiley‐Liss, Inc.     

Patterns of testosterone in male white‐tailed deer (Odocoileus virginianus): Seasonal and lifetime variation

Testosterone is strongly associated with the annual development of antlers in cervids, but endocrine research on wild, freely breeding ungulates is often done without repeated capture of known‐aged individuals. As a result, our knowledge on how testosterone fluctuates over the course of a lifetime and variation in lifetime patterns among individuals is limited. We investigated patterns of testosterone in a freely breeding population of white‐tailed deer (Odocoileus virginianus) in Alabama, USA, that breeds in January. Testosterone peaked during the height of the breeding season, despite this period occurring approximately 2 months later than in most temperate‐region white‐tailed deer populations. Age‐related differences in testosterone were only prevalent during the breeding season, with bucks ≥3.5 years old having greater testosterone (853 ng/dl ± 96 SE; p = 0.012) than bucks 1.5–2.5 years old (364 ng/dl ± 100 SE). Additionally, an individual''s testosterone level as a yearling was not positively associated with their lifetime maximum testosterone level (p = 0.583), and an individual''s mean testosterone level was positively associated with lifetime testosterone variation (p < 0.001). To our knowledge, our study is one of the first to assess how testosterone early in life might relate to individual testosterone later in life. We believe these data provide insight into lifetime hormonal patterns in cervids, and that these patterns may indicate intraspecific variation of lifetime reproductive strategies.     

Reproductive patterns in pygmy lorises (Nycticebus pygmaeus): Behavioral and physiological correlates of gonadal activity

The purpose of this study was to evaluate behavioral and physiological parameters of reproduction in a breeding colony of pygmy lorises. To this end, nine male and eight female adult pygmy lorises were kept under natural lighting conditions and monitored through five consecutive breeding seasons. Behavioral data were collected continuously throughout the year on all loris pairs. Behaviors associated with estrogen peaks in females included approaches, leaves, and lunges by females. Whistles were more frequent during estrus, but there was high inter‐individual variability. Males responded to estrous females by persistent following. There was a higher percentage of births in pairs that were together for more than 30 days before onset of estrus, compared with pairs that were put together when females came into estrus. However, these results may have been influenced by factors such as previous familiarity and social compatibility. Fecal testosterone levels were measured using radioimmunoassays and correlated with estrogen peaks and labial swelling of the females. The data showed an annual rhythm in testosterone that was consistent with a July–August mating season. Captive births were significantly higher during January–April than they were during any other months of the year. The earliest testosterone peak in a juvenile male was detected at 58 weeks, while the youngest male to sire offspring was 73 weeks of age at the time of the conception. Zoo Biol 22:15–32, 2003. © 2003 Wiley‐Liss, Inc.     

Individual variation in testosterone and parental care in a female songbird; The dark-eyed junco (Junco hyemalis)

When competition for sex-specific resources overlaps in time with offspring production and care, trade-offs can occur. Steroid hormones, particularly testosterone (T), play a crucial role in mediating such trade-offs in males, often increasing competitive behaviors while decreasing paternal behavior. Recent research has shown that females also face such trade-offs; however, we know little about the role of T in mediating female phenotypes in general, and the role of T in mediating trade-offs in females in particular. Here we examine the relationship between individual variation in maternal effort and endogenous T in the dark-eyed junco, a common songbird. Specifically, we measure circulating T before and after a physiological challenge (injection of gonadotropin releasing hormone, GnRH), and determine whether either measure is related to provisioning, brooding, or the amount of T sequestered in egg yolk. We found that females producing more T in response to a challenge spent less time brooding nestlings, but provisioned nestlings more frequently, and deposited more T in their eggs. These findings suggest that, while T is likely important in mediating maternal phenotypes and female life history tradeoffs, the direction of the relationships between T and phenotype may differ from what is generally observed in males, and that high levels of endogenous T are not necessarily as costly as previous work might suggest.     

Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae)

In the protogynous stoplight parrotfish (Sparisoma viride), large males defend territories that encompass the home-ranges of several mature females. However, high-quality habitat is in short supply, such that smaller, competitively inferior males do not defend territories. We investigated the role of 11-ketotestosterone (11KT) and testosterone (T) in the regulation of territorial behavior in a wild population of a protogynous reef fish, the stoplight parrotfish, at Glover's Reef, Belize. Radioimmunoassay of plasma samples from individuals of known social status revealed that nonterritorial males have lower levels of T and 11KT than territorial males. Nonterritorial males allowed access to vacant territories underwent pronounced increases in T and 11KT. When sampled 1 week after territory acquisition, levels of T and 11KT in new territorial males were significantly higher than the levels in established territorial males, but by 3 weeks after territory acquisition, there was no significant difference. We further investigated the hypothesis that such short-term increases in androgen levels are a response to intense male-male interactions during territory establishment. Simulated territorial intrusion promoted increased plasma levels of both T and 11KT while access to vacant territories without neighboring territorial males did not. These findings suggest that the endocrine system plays a role in fine-tuning the levels of territorial aggression exhibited by male stoplight parrotfish. We discuss these results in light of recent theory in behavioral endocrinology.