An Interactive Feeder to Induce and Assess Emotions from Vocalisations of Chickens.

Understanding the emotional states of animals is a long-standing research endeavour that has clear applications in animal welfare. Vocalisations are emerging as a promising way to assess both positive and negative emotional states. However, the vocal expression of emotions in birds is a relatively unexplored research area. The goal of this study was to develop an interactive feeding system that would elicit positive and negative emotional states, and collect recordings of the vocal expression of these emotions without human interference. In this paper, the mechatronic design and development of the feeder is described. Design choices were motivated by the desire for the hens to voluntarily interact with the feeder and experience the different stimuli that were designed to induce (1) positive low-arousal, (2) positive high-arousal, (3) negative low-arousal, and (4) negative high-arousal states. The results showed that hens were motivated to engage with the feeder despite the risk of receiving negative stimuli and that this motivation was sustained for at least 1 week. The potential of using the interactive feeder to analyse chicken vocalisations related to emotional valence and arousal is being explored, offering a novel proof of concept in animal welfare research. Preliminary findings suggest that hens vocalised in response to all four stimulus types, with the number of vocalisations, but not the probability of vocalising, distinguishing between low- and high-arousal states. Thus, the proposed animal-computer interaction design has potential to be used as an enrichment device and for future experiments on vocal emotions in birds.

Early life conditions reduce similarity between reproductive partners in HPA axis response to stress.

Social environments modulate endocrine function, yet it is unclear whether individuals can become like their social partners in how they physiologically respond to stressors. This social transmission of hypothalamic-pituitary-adrenal (HPA) axis reactivity could have long-term consequences for health and lifespan of individuals if their social partners react to stressors with an exaggerated HPA axis response. We tested whether glucocorticoid levels in response to stress of breeding partners changes after breeding depending on whether partners had similar or dissimilar postnatal conditions. We manipulated postnatal conditions by mimicking early life stress in zebra finch chicks (Taeniopygia guttata) via postnatal corticosterone exposure. When they reached adulthood, we created breeding pairs where the female and male had experienced either the same or different early life hormonal treatment (corticosterone or control). Before and after breeding, we obtained blood samples within 3 min and after 10 min or 30 min of restraint stress (baseline, cort10, cort30). We found that corticosterone levels of individuals in response to restraint were affected by their own and their partner's early life conditions, but did not change after breeding. However, across all pairs, partners became more similar in cort30 levels after breeding, although differences between partners in cort10 remained greater in pairs with a corticosterone-treated female. Thus, we show that HPA axis response to stressors in adulthood can be modulated by reproductive partners and that similarity between partners is reduced when females are postnatally exposed to elevated glucocorticoids.

The multi-dimensional nature of vocal learning.

How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav.60, 1-11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci.4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Learning strategies and the social brain: Missing elements in the link between developmental stress, song and cognition?

Bird songs may advertise aspects of cognition because song learning and learning speed in cognitive tasks are both affected by early-life environments. However, such relationships remain ambiguous in the literature. Here, I discuss 2 lines of research that may help to demystify links between song learning and cognition. First, learning strategies should be considered when assessing performance to ensure that individual differences in learning ability are not masked by individual differences in learning strategies. Second, song characteristics should be associated with social behavior because songs have a social purpose and, consequently, should be strongly related at functional and neural levels. Finally, if song learning and cognitive abilities are correlated because they develop concurrently and/or share or compete for the same resources, I discuss ways glucocorticoids may link early-life stress, song learning and cognitive ability, focusing particularly on oxidative stress as a potential mechanism.

Vocal tract constancy in birds and humans.

Humans perceive speech as being relatively stable despite acoustic variation caused by vocal tract (VT) differences between speakers. Humans use perceptual 'vocal tract normalisation' (VTN) and other processes to achieve this stability. Similarity in vocal apparatus/acoustics between birds and humans means that birds might also experience VT variation. This has the potential to impede bird communication. No known studies have explicitly examined this, but a number of studies show perceptual stability or 'perceptual constancy' in birds similar to that seen in humans when dealing with VT variation. This review explores similarities between birds and humans and concludes that birds show sufficient evidence of perceptual constancy to warrant further research in this area. Future work should 1) quantify the multiple sources of variation in bird vocalisations, including, but not limited to VT variations, 2) determine whether vocalisations are perniciously disrupted by any of these and 3) investigate how birds reduce variation to maintain perceptual constancy and perceptual efficiency.

Directional Asymmetries in Vowel Perception of Adult Nonnative Listeners Do Not Change Over Time With Language Experience.

Purpose: This study tested an assumption of the Natural Referent Vowel (Polka & Bohn, 2011) framework, namely, that directional asymmetries in adult vowel perception can be influenced by language experience. Method: Data from participants reported in Escudero and Williams (2014) were analyzed. Spanish participants categorized the Dutch vowels /aː/ and /ɑ/ in 2 separate sessions: before and after vowel distributional training. Sessions were 12 months apart. Categorization was assessed using the XAB task, where on each trial participants heard 3 sounds sequentially (first X, then A, then B) and had to decide whether X was more similar to A or B. Results: Before training, participants exhibited a directional asymmetry in line with the prediction of Natural Referent Vowel. Specifically, Spanish listeners performed worse when the vowel change from X to A was a change from peripheral to central vowel (/ɑ/ to /aː/). However, this asymmetry was maintained 12 months later, even though distributional training improved vowel categorization performance. Conclusions: Improvements in adult nonnative vowel categorization accuracy are not explained by attenuation of directional asymmetries. Directional asymmetries in vowel perception are altered during native language acquisition, but may possibly be impervious to nonnative language experiences in adulthood.

Speaker and Accent Variation Are Handled Differently: Evidence in Native and Non-Native Listeners.

Listeners are able to cope with between-speaker variability in speech that stems from anatomical sources (i.e. individual and sex differences in vocal tract size) and sociolinguistic sources (i.e. accents). We hypothesized that listeners adapt to these two types of variation differently because prior work indicates that adapting to speaker/sex variability may occur pre-lexically while adapting to accent variability may require learning from attention to explicit cues (i.e. feedback). In Experiment 1, we tested our hypothesis by training native Dutch listeners and Australian-English (AusE) listeners without any experience with Dutch or Flemish to discriminate between the Dutch vowels /I/ and /ε/ from a single speaker. We then tested their ability to classify /I/ and /ε/ vowels of a novel Dutch speaker (i.e. speaker or sex change only), or vowels of a novel Flemish speaker (i.e. speaker or sex change plus accent change). We found that both Dutch and AusE listeners could successfully categorize vowels if the change involved a speaker/sex change, but not if the change involved an accent change. When AusE listeners were given feedback on their categorization responses to the novel speaker in Experiment 2, they were able to successfully categorize vowels involving an accent change. These results suggest that adapting to accents may be a two-step process, whereby the first step involves adapting to speaker differences at a pre-lexical level, and the second step involves adapting to accent differences at a contextual level, where listeners have access to word meaning or are given feedback that allows them to appropriately adjust their perceptual category boundaries.

A general auditory bias for handling speaker variability in speech? Evidence in humans and songbirds.

Different speakers produce the same speech sound differently, yet listeners are still able to reliably identify the speech sound. How listeners can adjust their perception to compensate for speaker differences in speech, and whether these compensatory processes are unique only to humans, is still not fully understood. In this study we compare the ability of humans and zebra finches to categorize vowels despite speaker variation in speech in order to test the hypothesis that accommodating speaker and gender differences in isolated vowels can be achieved without prior experience with speaker-related variability. Using a behavioral Go/No-go task and identical stimuli, we compared Australian English adults' (naïve to Dutch) and zebra finches' (naïve to human speech) ability to categorize / I/ and /ε/ vowels of an novel Dutch speaker after learning to discriminate those vowels from only one other speaker. Experiments 1 and 2 presented vowels of two speakers interspersed or blocked, respectively. Results demonstrate that categorization of vowels is possible without prior exposure to speaker-related variability in speech for zebra finches, and in non-native vowel categories for humans. Therefore, this study is the first to provide evidence for what might be a species-shared auditory bias that may supersede speaker-related information during vowel categorization. It additionally provides behavioral evidence contradicting a prior hypothesis that accommodation of speaker differences is achieved via the use of formant ratios. Therefore, investigations of alternative accounts of vowel normalization that incorporate the possibility of an auditory bias for disregarding inter-speaker variability are warranted.

Transient and permanent effects of suboptimal incubation temperatures on growth, metabolic rate, immune function and adrenocortical responses in zebra finches.

In birds, incubation temperature can vary by several degrees Celsius among nests of a given species. Parents may alter incubation temperature to cope with environmental conditions and/or to manipulate embryonic development, and such changes in incubation behavior could have long-lasting effects on offspring phenotype. To investigate short- and long-term effects of suboptimal incubation temperatures on survival and physiological functions in zebra finches, eggs were incubated at 36.2, 37.4 or 38.4 °C for the entire incubation period. The post-hatch environment was identical among the treatment groups. We found that hatching success was lowest in the 38.4 °C group, while post-hatch survival was lowest in the 36.2 °C group. Incubation temperature had sex-specific effects on offspring phenotype: incubation temperatures affected body mass (Mb) but not physiological parameters of males and conversely, the physiological parameters but not Mb of females. Specifically, males from the 38.4 °C group weighed significantly less than males from the 36.2 °C group from the nestling period to adulthood, whereas females from different incubation temperature groups did not differ in Mb. In contrast, females incubated at 36.2 °C had transient but significantly elevated basal metabolic rate and adrenocortical responses during the nestling and fledgling periods, whereas no treatment effect was observed in males. Innate immunity was not affected by incubation temperature in either sex. These results suggest that a 1 °C deviation from what is considered an optimal incubation temperature can lower offspring performance and offspring survival.

No Trade-Offs between Lipid Stores and Structural Growth in Juvenile Zebra Finches Undergoing Nutritional Stress during Development.

Nutritional conditions during development can affect both structural growth and body fat deposition. Body size and body fat each have significant consequences for fitness, yet few studies have investigated how young birds balance resource allocation between structural growth and fat reserves. We raised zebra finches (Taeniopygia guttata) in consistently high- or low-food conditions until posthatch day 35 (PHD 35). From this age until PHD 62, half of the birds in each condition were switched to the other treatment, while the rest were maintained on the same conditions. Body mass, lean mass, body fat, and tarsus length were measured before (PHD 25) and after (PHD 55) nutritional independence. Precise measures of body composition were obtained noninvasively at both ages using quantitative magnetic resonance analysis. At PHD 25, birds in the high treatment had more body mass and lean mass than birds in the low treatment, but nutritional treatments did not affect body fat at this age. Unexpectedly, the strategic response of birds that experienced deteriorating food availability was to maintain body mass by increasing body fat and decreasing lean mass. Birds that experienced an improvement in food availability significantly increased body mass by increasing lean mass and not body fat. Birds maintained on a low diet throughout did not significantly increase body mass, lean mass, or body fat. Tarsus length was not affected by nutritional manipulations. These findings indicate that nutritional stress did not affect the relationship between skeletal growth and body fat deposition because lean mass, body fat, and tarsus length can be independently regulated at different developmental periods depending on nutritional conditions.

Revisiting vocal perception in non-human animals: a review of vowel discrimination, speaker voice recognition, and speaker normalization.

The extent to which human speech perception evolved by taking advantage of predispositions and pre-existing features of vertebrate auditory and cognitive systems remains a central question in the evolution of speech. This paper reviews asymmetries in vowel perception, speaker voice recognition, and speaker normalization in non-human animals - topics that have not been thoroughly discussed in relation to the abilities of non-human animals, but are nonetheless important aspects of vocal perception. Throughout this paper we demonstrate that addressing these issues in non-human animals is relevant and worthwhile because many non-human animals must deal with similar issues in their natural environment. That is, they must also discriminate between similar-sounding vocalizations, determine signaler identity from vocalizations, and resolve signaler-dependent variation in vocalizations from conspecifics. Overall, we find that, although plausible, the current evidence is insufficiently strong to conclude that directional asymmetries in vowel perception are specific to humans, or that non-human animals can use voice characteristics to recognize human individuals. However, we do find some indication that non-human animals can normalize speaker differences. Accordingly, we identify avenues for future research that would greatly improve and advance our understanding of these topics.

Juvenile nutritional stress affects growth rate, adult organ mass, and innate immune function in zebra finches (Taeniopygia guttata).

Developmental conditions may influence many aspects of adult phenotype, including growth and immune function. Whether poor developmental environments impair both growth and immune function or induce a trade-off between the two processes is inconclusive, and the impact of the timing of stress in determining this relationship has so far been overlooked. We tested the hypothesis that the long-term effects of nutritional stress on growth, body composition, and immune function in zebra finches (Taeniopygia guttata) are different depending on whether stress is experienced during an early or a juvenile phase (i.e., before or after nutritional independence, respectively). We raised birds on high (H) or low (L) food conditions until posthatch day (PHD) 35 and switched treatments for half of the birds in each of the H and L groups from PHD 36 to 61. We found that unfavorable juvenile conditions (PHD 36-61) increased somatic growth rates and liver mass, body fat, and some aspects of immune function. We also observed a positive relationship between growth and immune function, as individuals that grew faster as juveniles also had better innate immune responses as adults. There was no effect of treatment on basal metabolic rate. These findings demonstrate the importance of juvenile developmental conditions in shaping multiple aspects of the adult phenotype.

Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system.

Chronic elevations in glucocorticoids can decrease the production and survival of new cells in the adult brain. In rat hippocampus, supraphysiological doses of dehydroepiandrosterone (DHEA; a sex steroid precursor synthesized in the gonads, adrenals, and brain) have antiglucocorticoid properties. With male song sparrows (Melospiza melodia), we examined the effects of physiological doses of corticosterone, the primary circulating glucocorticoid in birds, and DHEA on adult neuroplasticity. We treated four groups of nonbreeding sparrows for 28 days with empty (control), corticosterone, DHEA, or corticosterone + DHEA implants. Subjects were injected with BrdU on days 3 and 4. In HVC, a critical song control nucleus, corticosterone and DHEA had independent, additive effects. Corticosterone decreased, whereas DHEA increased, HVC volume, NeuN(+) cell number, and BrdU(+) cell number. Coadministration of DHEA completely reversed the neurodegenerative effects of chronic corticosterone treatment. In an efferent target of HVC, the robust nucleus of the arcopallium (RA), DHEA increased RA volume, but this effect was blocked by coadministration of corticosterone. There were similar antagonistic interactions between corticosterone and DHEA on BrdU(+) cell number in the hippocampus and ventricular zone. This is the first report on the effects of corticosterone treatment on the adult song control circuit, and HVC was the most corticosterone-sensitive song nucleus examined. In HVC, DHEA is neuroprotective and counteracts several pronounced effects of corticosterone. Within brain regions that are particularly vulnerable to corticosterone, such as the songbird HVC and rat hippocampus, DHEA appears to be a potent native antiglucocorticoid.