Hearing and vocalizations in a small songbird, the red-cheeked cordon bleu (Uraeginthus bengalus) (L).

The auditory sensitivity of a small songbird, the red-cheeked cordon bleu, was measured using the standard methods of animal psychophysics. Hearing in cordon bleus is similar to other small passerines with best hearing in the frequency region from 2 to 4 kHz and sensitivity declining at the rate of about 10 dB/octave below 2 kHz and about 35 dB/octave as frequency increases from 4 to 9 kHz. While critical ratios are similar to other songbirds, the long-term average power spectrum of cordon bleu song falls above the frequency of best hearing in this species.

Male and female red-cheeked cordon bleus sing similar yet individualistic songs.

Birdsong is an excellent system for studying complex vocal signaling in both males and females. Historically, most research in captivity has focused only on male song. This has left a gap in our understanding of the environmental, neuroendocrine, and mechanistic control of female song. Here, we report the overall acoustic features, repertoire, and stereotypy of both male and female Red-Cheeked Cordon Bleus (Uraeginthus bengalus) (RCCBs) songs in the lab. We found few sex differences in the acoustic structure, song repertoire, and song stereotypy of RCCBs. Both sexes had similar song entropy, peak frequency, and duration. Additionally, individuals of both sexes sang only a single song type each and had similar levels of song and syllable stereotypy. However, we did find that female RCCBs had higher song bandwidth but lower syllable repertoires. Finally, and most strikingly, we found highly individualistic songs in RCCBs. Each individual produced a stereotyped and unique song with no birds sharing song types and very few syllable types being shared between birds of either sex. We propose that RCCBs represent a promising species for future investigations of the acoustic sex differences in song in a lab environment, and also for understanding the evolutionary driving forces behind individualistic songs.

Song system neuroanatomy, and immediate early gene expression in a finch species with extensive male and female song.

Birdsong is a relatively well-studied behavior, both due to its importance as a model for vocal production learning and as an intriguing complex social behavior. Until the last few decades, work on birdsong focused almost exclusively on males. However, it is now widely accepted that female song not only exists, but is fairly common throughout the oscine passerines. Despite this, and the large number of researchers who have begun exploring female song in the field, researchers in the lab have been slow to adopt model species with female song. Studying female song in the lab is critical for our understanding of sex-specific factors in the physiology controlling this fascinating behavior. Additionally, as a model for vocal production learning in humans, understanding the mechanistic and neuroendocrine control of female song is clearly important. In this study, we examined the red-cheeked cordon bleu (RCCB), an Estrildid finch species with extensive female song. Specifically, we found that there were no significant sex differences in circulating levels of testosterone and progesterone, nor in song production rate. There were no significant differences in cell densities in the three nuclei of the song control system we examined. Additionally, the volume of the robust nucleus of the arcopallium was not significantly different and we report the smallest sex difference in HVC yet published in a songbird. Finally, we demonstrated similar levels of motor driven immediate early gene expression in both males and females after song production.

Sex differences in seasonal brain plasticity and the neuroendocrine regulation of vocal behavior in songbirds.

Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neuroendocrine control has been primarily studied in male songbirds in both laboratory studies of captive birds and field studies of wild caught birds. The bias toward studying seasonality in the neuroendocrine regulation of song in male birds comes from a historic focus on sexually selected male behaviors. In fact, given that male song is often loud and accompanied by somewhat extravagant courtship behaviors, female song has long been overlooked. To compound this bias, the primary model songbird species for studies in the lab, zebra finches (Taeniopygia guttata) and canaries (Serinus canaria), exhibit little or no female song. Therefore, understanding the degree of variation and neuroendocrine control of seasonality in female songbirds is a major gap in our knowledge. In this review, we discuss the importance of studying sex differences in seasonal plasticity and the song control system. Specifically, we discuss sex differences in 1) the neuroanatomy of the song control system, 2) the distribution of receptors for androgens and estrogens and 3) the seasonal neuroplasticity of the hypothalamo-pituitary-gonadal axis as well as in the neural and cellular mechanisms mediating song system changes. We also discuss how these neuroendocrine mechanisms drive sex differences in seasonal behavior. Finally, we highlight specific gaps in our knowledge and suggest experiments critical for filling these gaps.

Neuroendocrine and behavioral response to testosterone-induced female song in canaries (Serinus canaria).

Male song in songbirds is a critical and elaborate signal for mate attraction. In many species female listeners respond to male song both behaviorally and physiologically (e.g. copulation solicitation displays and production of the immediate early gene ZENK in auditory regions). It is becoming increasingly well known that females in many species also sing. However, in common lab species, such as canaries (Serinus canaria), female song is limited and has been primarily studied in the context of administering of exogenous testosterone (T) to increase song rate and length. In this study we addressed to what extent female canary songs are masculinized by the administration of exogenous T based on the behavioral and physiological responses of avian receivers. Specifically, are T induced female songs sufficient to elicit courtship behaviors and auditory ZENK expression in female listeners? We found that female songs after 3 weeks of exogenous T were significantly longer and more complex than female songs after 12 weeks of exogenous T. Additionally, we found that playback of 3-week T song significantly increased sexual response behaviors and the expression of ZENK in the auditory brain regions of female listeners. Finally, we conclude that extended periods of T do not necessarily maintain the masculinization of female song.

The singing question: re-conceptualizing birdsong.

Birdsong has been the subject of broad research from a variety of sub-disciplines and has taught us much about the evolution, function, and mechanisms driving animal communication and cognition. Typically, birdsong refers to the specialized vocalizations produced by oscines. Historically, much of the research on birdsong was conducted in north temperate regions (specifically in Europe and North America) leading to multiple biases. Due to these historic biases these vocalizations are generally considered to be highly sexually dimorphic, heavily shaped by sexual selection and essential for courtship and territoriality. Song is also typically defined as a learned trait shaped by cultural evolution. Together, this framework focuses research specifically on males, particularly during the north temperate breeding season - reflecting and thereby reinforcing this framework. The physiological underpinnings of song often emphasize the role of the hypothalamic-pituitary-gonadal axis (associated with breeding changes) and the song control system (underlying vocal learning). Over the years there has been great debate over which features of song are essential to the definition of birdsong, which features apply broadly to contexts outside males in the north temperate region, and over the importance of having a definition at all. Importantly, the definitions we use can both guide and limit the progress of research. Here, we describe the history of these definitions, and how these definitions have directed and restricted research to focus on male song in sexually selected contexts. Additionally, we highlight the gaps in our scientific knowledge, especially with respect to the function and physiological mechanisms underlying song in females and in winter, as well as in non-seasonally breeding species. Furthermore, we highlight the problems with using complexity and learning as dichotomous variables to categorize songs and calls. Across species, no one characteristic of song - sexual dimorphism, seasonality, complexity, sexual selection, learning - consistently delineates song from other songbird vocal communication. We provide recommendations for next steps to build an inclusive information framework that will allow researchers to explore nuances in animal communication and promote comparative research. Specifically, we recommend that researchers should operationalize the axis of variation most relevant to their study/species by identifying their specific question and the variable(s) of focus (e.g. seasonality). Researchers should also identify the axis (axes) of variation (e.g. degree of control by testosterone) most relevant to their study and use language consistent with the question and axis (axes) of variation (e.g. control by testosterone in the seasonal vocal production of birds).