Ostrich (Struthio camelus) syrinx morphology and vocal repertoire across postnatal ontogeny and sex: Implications for understanding vocal evolution in birds.

Vocal production in birds has been the target of considerable research that mostly has focused on phylogenetically well-nested songbirds. Anatomical descriptions and recordings of many non-songbirds have often only focused on a single ontogenetic stage or sex. While basic morphology of the vocal organ (syrinx) of ostrich (Palaeognathae, Struthio camelus) has been known since the 1800s, descriptions of its vocal repertoire and syrinx anatomy since then have been incomplete or inconsistent. New toolkits now enable detailed qualitative description of internal anatomy and meristic data and allow it to be compared to vocal production. Here we describe the anatomy of the syrinx in Struthio camelus for three post-hatching ontogenetic stages and both an adult male and female utilizing dissection and contrast enhanced X-ray computed tomography (diceCT). We find changes in ring geometry and spacing through ontogeny as well as lateral labia thickness. We document a small unpaired, midline, cartilaginous structure, a "pessuliform process" at the tracheobronchial juncture present throughout ontogeny and in both males and females. Investigation of the vocal repertoire of ostriches across ontogeny using a new dataset of 77 recordings led to identification of four vocalizations not previously reported in the literature, including the simultaneous production of a hiss and tonal. We find syrinx morphology largely consistent across ontogeny and in male and female adults. Both are capable of producing long duration tonal calls, but these may be more frequent in male birds. Closed-mouth boom calls remain unique to males. A detailed understanding of diversity in parts of early diverging clades is pivotal in attempting to estimate features of the ancestral syrinx in birds and how avian vocalization evolved.

Oxytocin receptor antagonism during early vocal learning reduces song preference and imitation in zebra finches.

In species with vocal learning, acquiring species-typical vocalizations relies on early social orienting. In songbirds, for example, learning song requires dynamic social interactions with a "tutor" during an early sensitive period. Here, we hypothesized that the attentional and motivational processes that support song learning recruit the oxytocin system, which is well-understood to play a role in social orienting in other species. Juvenile male zebra finches naïve to song were each tutored by two unfamiliar adult males. Before exposure to one tutor, juveniles were injected subcutaneously with oxytocin receptor antagonist (OTA; ornithine vasotocin) and before exposure to the other, saline (control). Treatment with OTA reduced behaviors associated with approach and attention during tutoring sessions. Using a novel operant paradigm to measure preference while balancing exposure to the two tutor songs, we showed that the juveniles preferred to hear the song of the control tutor. Their adult songs more closely resembled the control tutor's song, and the magnitude of this difference was predicted by early preference for control over OTA song. Overall, oxytocin antagonism during exposure to a tutor seemed to bias juveniles against that tutor and his song. Our results suggest that oxytocin receptors are important for socially-guided vocal learning.

Song preferences predict the quality of vocal learning in zebra finches.

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we tested the hypothesis that during song learning, the reward value of hearing a particular song predicts the degree to which that song will ultimately be learned. We measured the early song preferences of young male zebra finches (Taeniopygia guttata) in an operant key-pressing assay; each of two keys was associated with a higher likelihood of playing the song of the father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a novel reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the father's song early during song learning, before actual singing occurs in this species. When they reached adulthood, all the birds copied the father's song. The accuracy with which the father's song was imitated was positively correlated with the peak strength of the preference for the father's song during the sensitive period of song learning. Our results show that preference for the song of a chosen tutor, in this case the father, predicted vocal learning during development.

High-frequency vocalizations in Andean hummingbirds.

Hummingbirds possess a number of unique features. A recent report in Current Biology[1] showed that the Black Jacobin (Florisuga fusca), a Brazilian hummingbird in the Topazes clade, produces high-frequency vocalizations outside the known hearing range of birds. Here, we report that four hummingbird species in the Andean clade [2,3] also exhibit high-frequency vocalizations: the Ecuadorian Hillstar (Oreotrochilus chimborazo), with the highest fundamental frequency (mean F0 = 13.4 kHz), the Buff-tailed Coronet (Boissonneaua flavescens), Speckled Hummingbird (Adelomyia melanogenys) and Violet-tailed Sylph (Aglaiocercus coelestis). The presence of high-frequency vocalizations in hummingbirds belonging to different lineages poses the question of whether high-frequency vocalizations in this group of birds have been, so far, overlooked. These Andean species are closely related but live in two different habitats. Our characterization of ambient noise in each habitat suggests that the hummingbirds are exposed to different acoustic challenges, and that the frequency content of the vocalizations of the cloud-forest species is adapted accordingly. The function of these signals and the selection pressures driving their evolution remain unknown.

Sound-induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally-breeding songbird.

Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally-breeding female songbirds, for example, sound-induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma estradiol reaches breeding-like levels. This selectivity has been hypothesized to be mediated by release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen-primed female white-throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. In order to mediate hormone-dependent selectivity, this release must be (1) selective for song and (2) modulated by endocrine state. Therefore, in the current study we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or non-breeding endocrine state. We then used high performance liquid chromatography to measure turnover of dopamine, norepinephrine, and serotonin in the auditory midbrain and forebrain. We found that sound-induced turnover of dopamine and serotonin did in fact depend on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding-like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound-induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a non-breeding endocrine state. Our results suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated. This article is protected by copyright. All rights reserved.

To Become Senders, Songbirds Must be Receivers First.

Courtship signals are attractive; in other words, receivers are motivated to approach courtship signals. Though the concept of a receiver is commonly associated in the literature with that of a mate seeker, young songbirds that are learning to sing by imitating conspecifics are also receivers. Juvenile songbirds are attracted to conspecific songs, which has been shown by juveniles working to hear song in operant chambers. The mechanisms explaining this attraction are poorly understood. Here, I review studies that hint at the mechanisms by which conspecific song becomes attractive. In at least some species, juveniles imitate individuals with which they have a strong social bond, such as the father. Such cases suggest that social reward plays a role in the process of song becoming attractive. In addition, experiments using birds reared in isolation from conspecific song have shown that juveniles imitate songs that have acoustic features that are typically found in conspecific song. Those studies suggest that such features are attractive to juveniles regardless of their social experience. The relative contributions of social reward and species-typical acoustic features to the attractiveness of a song can be determined using methods such as operant conditioning. For example, juvenile songbirds can be given control over the playback of songs that differ in a given attribute, such as acoustic similarity to the song of the father. The juveniles will frequently elicit playback of the songs that are attractive to them. Investigating the mechanisms that contribute to the attractiveness of conspecific song to learners will broaden our understanding of the evolution of song as a courtship signal, because the preferences of learners may ultimately determine what will be sung to potential mates.

Testosterone and Haemosporidian Parasites Along a Tropical Elevational Gradient in Rufous-Collared Sparrows (Zonotrichia capensis).

Elevation has been proposed as a dominant ecological variable shaping life history traits and subsequently their underlying hormonal mechanisms. In an earlier meta-analysis of tropical birds, elevation was positively related to testosterone levels. Furthermore, parasitism by avian haemosporidians should vary with elevation as environmental conditions affect vector abundance, and while testosterone is needed for breeding, it is hypothesized to be immunosuppressive and thus could exacerbate haemosporidian infection. Our objective in this study was to examine the relationships between elevation, testosterone levels, and parasitism by avian haemosporidians. We surveyed breeding male rufous-collared sparrows (Zonotrichia capensis) across a wide elevational range along the equator. We measured baseline testosterone levels, haemosporidian infection at four elevations spanning the species' natural range in the Ecuadorian Andes (600, 1500, 2100, 3300 m). Testosterone levels from breeding males were not related to elevation, but there was high intrapopulation variability. Testosterone levels were not related to the probability of parasitism, but our results from one population suggested that the likelihood of being infected by haemosporidian parasites was greater when in breeding condition. In conclusion, even though there is variation in life history strategies among the studied populations, wider divergence in seasonality and life history traits would probably be needed to detect an effect of elevation on testosterone if one exists. Additionally, our results show that variation in testosterone is not related to infection risk of haemosporidians, thus other factors that take a toll on energetic resources, such as reproduction, should be looked at more closely.