Resource allocation across the egg laying sequence in the wild zebra finch Taeniopygia guttata

Zebra finches have played a central role in the discovery of a variety of maternal effects over the past decade, with females shown to adjust resource allocation to their eggs in response to variables such as the appearance of their partner, their own condition, and the diet on which they are maintained. In addition to being the focus of some of the most high profile individual studies that have influenced maternal effects research in birds, the multitude of zebra finch studies together provide the most comprehensive set of data to illuminate general patterns and compare different maternally derived variables. Surprisingly, to date, virtually all of this work has focused on captive populations of the zebra finch that have been domesticated for many generations, and which are typically held under relatively constant environmental and dietary conditions. Here we report the first data on resource allocation across the egg laying sequence in a free-living wild population. Reassuringly we find that the patterns that have been found in the majority of studies of domesticated populations with respect to investment across the laying sequence were all present in the wild population. The size and mass of eggs increased through the laying sequence whilst the concentration of carotenoids significantly decreased across the laying sequence. Although there was no significant pattern with respect to testosterone across the laying sequence the first two eggs had a higher level of testosterone than the last few eggs in the clutch, which is also consistent with the findings of earlier studies in captive populations. © 2011 The Authors.

Sex steroid profiles and pair-maintenance behavior of captive wild-caught zebra finches (taeniopygia guttata)

Here, we studied the life-long monogamous zebra finch, to examine the relationship between circulating sex steroid profiles and pair-maintenance behavior in pairs of wild-caught zebra finches (paired in the laboratory for >1 month). We used liquid chromatography-tandem mass spectrometry to examine a total of eight androgens and progestins [pregnenolone, progesterone, dehydroepiandrosterone (DHEA), androstenediol, pregnan-3,17-diol-20-one, androsterone, androstanediol, and testosterone]. In the plasma, only pregnenolone, progesterone, DHEA, and testosterone were above the limit of quantification. Sex steroid profiles were similar between males and females, with only circulating progesterone levels significantly different between the sexes (female > male). Circulating pregnenolone levels were high in both sexes, suggesting that pregnenolone might serve as a circulating prohormone for local steroid synthesis in zebra finches. Furthermore, circulating testosterone levels were extremely low in both sexes. Additionally, we found no correlations between circulating steroid levels and pair-maintenance behavior. Taken together, our data raise several interesting questions about the neuroendocrinology of zebra finches.

L’influence des capacités cognitives mâles et femelles sur le choix de partenaire chez le diamant mandarin (Taeniopygia guttata)

S’approvisionner en nourriture est essentiel à la survie et au succès reproducteur. Lorsque les animaux font face à des changements environnementaux brutaux, ils doivent s’ajuster rapidement à leur nouvel environnement et parfois même innover dans leur façon de s’approvisionner. Des processus comportementaux et cognitifs, tels que l’innovation et l’apprentissage, permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental afin de s'adapter de façon optimale. Les performances cognitives varient entre les individus d’une même population et bien que des études récentes se soient intéressées aux causes de ce phénomène, de convaincantes évidences sont manquantes afin d’expliquer pourquoi ces variations sont maintenues. Au cours de ce mémoire, les questions des pressions de sélection s'exerçant sur les performances d’alimentation par une tâche motrice nouvelle sont abordées afin de mieux comprendre l'évolution des capacités cognitives au sein d'une population captive de diamants mandarins (Taeniopygia guttata). Nous avons tout d'abord testé si les femelles diamants mandarins modifient leurs préférences d'accouplement après avoir observé la performance d'alimentation par une tâche motrice nouvelle des mâles. Afin de déterminer si les femelles sont capables de discriminer entre les mâles sur la base de leur capacité cognitive, nous avons également évalué les performances d’apprentissage de chacune d’elles. En effet, des études ont suggéré qu’il peut être coûteux, spécialement en terme de temps, de discriminer entre des partenaires potentiels sur cette base. La généralisation d’une préférence pour un mâle performant à d’autres mâles possédant le même phénotype permettrait la réduction de ces coûts. Nous avons donc finalement testé si les femelles diamants mandarins peuvent généraliser leur préférence après avoir observé les performances d’alimentation pour une tâche motrice nouvelle d’un mâle. Nos résultats suggèrent que les femelles diamants mandarins ne peuvent évaluer les capacités cognitives d’un mâle par l’intermédiaire de traits indicateurs. Toutefois, nous avons démontré qu’une observation directe des performances d’alimentation d’un mâle guide le choix d’appariement des femelles. Également, nous avons montré que les femelles peuvent généraliser l’apparence du mâle le plus performant et utiliser cette information lors de l’évaluation de nouveaux mâles. La relation entre les performances cognitives et le choix de partenaire pourraient s’expliquer par exemple par une meilleure exploitation de l’habitat, mais nécessite des études plus approfondies.

L’influence des capacités cognitives mâles et femelles sur le choix de partenaire chez le diamant mandarin (Taeniopygia guttata)

S’approvisionner en nourriture est essentiel à la survie et au succès reproducteur. Lorsque les animaux font face à des changements environnementaux brutaux, ils doivent s’ajuster rapidement à leur nouvel environnement et parfois même innover dans leur façon de s’approvisionner. Des processus comportementaux et cognitifs, tels que l’innovation et l’apprentissage, permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental afin de s'adapter de façon optimale. Les performances cognitives varient entre les individus d’une même population et bien que des études récentes se soient intéressées aux causes de ce phénomène, de convaincantes évidences sont manquantes afin d’expliquer pourquoi ces variations sont maintenues. Au cours de ce mémoire, les questions des pressions de sélection s'exerçant sur les performances d’alimentation par une tâche motrice nouvelle sont abordées afin de mieux comprendre l'évolution des capacités cognitives au sein d'une population captive de diamants mandarins (Taeniopygia guttata). Nous avons tout d'abord testé si les femelles diamants mandarins modifient leurs préférences d'accouplement après avoir observé la performance d'alimentation par une tâche motrice nouvelle des mâles. Afin de déterminer si les femelles sont capables de discriminer entre les mâles sur la base de leur capacité cognitive, nous avons également évalué les performances d’apprentissage de chacune d’elles. En effet, des études ont suggéré qu’il peut être coûteux, spécialement en terme de temps, de discriminer entre des partenaires potentiels sur cette base. La généralisation d’une préférence pour un mâle performant à d’autres mâles possédant le même phénotype permettrait la réduction de ces coûts. Nous avons donc finalement testé si les femelles diamants mandarins peuvent généraliser leur préférence après avoir observé les performances d’alimentation pour une tâche motrice nouvelle d’un mâle. Nos résultats suggèrent que les femelles diamants mandarins ne peuvent évaluer les capacités cognitives d’un mâle par l’intermédiaire de traits indicateurs. Toutefois, nous avons démontré qu’une observation directe des performances d’alimentation d’un mâle guide le choix d’appariement des femelles. Également, nous avons montré que les femelles peuvent généraliser l’apparence du mâle le plus performant et utiliser cette information lors de l’évaluation de nouveaux mâles. La relation entre les performances cognitives et le choix de partenaire pourraient s’expliquer par exemple par une meilleure exploitation de l’habitat, mais nécessite des études plus approfondies.

Imaging Learned Song Representations in Populations of Sensorimotor Neurons Essential to Vocal Communication

Perceiving or producing complex vocalizations such as speech and birdsongs require the coordinated activity of neuronal populations, and these activity patterns can vary over space and time. How learned communication signals are represented by populations of sensorimotor neurons essential to vocal perception and production remains poorly understood. Using a combination of two-photon calcium imaging, intracellular electrophysiological recording and retrograde tracing methods in anesthetized adult male zebra finches (Taeniopygia guttata), I addressed how the bird's own song and its component syllables are represented by the spatiotemporal patterns of activity of two spatially intermingled populations of projection neurons (PNs) in HVC, a sensorimotor area required for song perception and production. These experiments revealed that neighboring PNs can respond at markedly different times to song playback and that different syllables activate spatially intermingled HVC PNs within a small region. Moreover, noise correlation analysis reveals enhanced functional connectivity between PNs that respond most strongly to the same syllable and also provides evidence of a spatial gradient of functional connectivity specific to PNs that project to song motor nucleus (i.e. HVC_RA cells). These findings support a model in which syllabic and temporal features of song are represented by spatially intermingled PNs functionally organized into cell- and syllable-type networks.

Listening in.

Zebra finches communicate with each other in ways that are more complex than previously thought.

Mitochondrial uncoupling as a regulator of life-history trajectories in birds: an experimental study in the zebra finch.

Mitochondria have a fundamental role in the transduction of energy from food into ATP. The coupling between food oxidation and ATP production is never perfect, but may nevertheless be of evolutionary significance. The 'uncoupling to survive' hypothesis suggests that 'mild' mitochondrial uncoupling evolved as a protective mechanism against the excessive production of damaging reactive oxygen species (ROS). Because resource allocation and ROS production are thought to shape animal life histories, alternative life-history trajectories might be driven by individual variation in the degree of mitochondrial uncoupling. We tested this hypothesis in a small bird species, the zebra finch (Taeniopygia guttata), by treating adults with the artificial mitochondrial uncoupler 2,4-dinitrophenol (DNP) over a 32-month period. In agreement with our expectations, the uncoupling treatment increased metabolic rate. However, we found no evidence that treated birds enjoyed lower oxidative stress levels or greater survival rates, in contrast to previous results in other taxa. In vitro experiments revealed lower sensitivity of ROS production to DNP in mitochondria isolated from skeletal muscles of zebra finch than mouse. In addition, we found significant reductions in the number of eggs laid and in the inflammatory immune response in treated birds. Altogether, our data suggest that the 'uncoupling to survive' hypothesis may not be applicable for zebra finches, presumably because of lower effects of mitochondrial uncoupling on mitochondrial ROS production in birds than in mammals. Nevertheless, mitochondrial uncoupling appeared to be a potential life-history regulator of traits such as fecundity and immunity at adulthood, even with food supplied ad libitum.

Les effets du lien social et du niveau de défense des ressources sur l’utilisation des tactiques producteur et chapardeur par les diamants mandarins

Plusieurs espèces s’alimentant en groupe ont un comportement correspondant au jeu producteur-chapardeur (P-C). Même si à l’origine ce jeu ne prenait pas en compte plusieurs éléments susceptibles d’être présents dans un groupe social, certaines études récentes suggèrent que des facteurs, notamment le niveau de défense des ressources et les liens sociaux, pourraient affecter ses prédictions. Notre étude avait pour but d’étudier les effets de ces facteurs en exposant des groupes de diamants mandarins à quatre traitements expérimentaux faisant varier la taille du groupe et le degré d’attachement des oiseaux. Notre étude est la première à montrer que le niveau de défense des ressources a un réel effet sur les fréquences d’utilisation des tactiques producteur et chapardeur. De fait, contrairement à ce qui est prédit dans le jeu P-C original, nous avons trouvé que la fréquence des chapardeurs n’augmente pas avec la taille du groupe dans un contexte favorisant la défense des ressources. Par ailleurs, nous n’avons pas trouvé d’effet significatif du lien social sur les fréquences d’utilisation des tactiques. Cependant, nos résultats suggèrent que les liens de couple changent le comportement individuel des sujets en ce qui a trait au chapardage et à l’agressivité : bien que le résultat soit non significatif, les individus chapardent davantage leur partenaire social que les autres membres du groupe, mais avec une agressivité plus faible. Les résultats obtenus sont prometteurs et ouvrent la voie à de nombreuses autres études sur l’effet des liens sociaux et la défense des ressources chez les espèces grégaires.

Mate choice in zebra finches: does corticosterone play a role?

The importance of stress as a factor in influencing life history strategies has received considerable attention in recent years, because it appears to have a substantial impact on an individual's behaviour and physiology. Birds respond to environmental and social stressors by the production of corticosterone, a glucocorticoid hormone released by the adrenal gland. In this experiment, we tested whether female zebra finches preferred males selected to produce low or high peak levels of circulating plasma corticosterone. Plasma corticosterone and testosterone levels of the males were recorded, as were morphometric measurements and perch activity. Spectrophotometric measurements were also taken from several putatively sexually selected regions of the males. The females preferred the males from the low corticosterone lines to the high corticosterone males. In addition to, and consistent with this effect, females preferred males with the lowest corticosterone titres. Male activity, testosterone level, body size and mass had no effect on female preference. Leg and beak brightness were important, however, as were the brightness and chromaticity of the male cheek patch. These results are discussed in relation to contemporary hypotheses in sexual selection, particularly in the context of stress-mediated signalling.

Plasma cholinesterase characteristics in native Australian birds : significance for monitoring avian species for pesticide exposure

Cholinesterase-inhibiting pesticides are applied throughout Australia to control agricultural pests. Blood plasma cholinesterase (ChE) activity is a sensitive indicator of exposure to organophosphorus insecticides in vertebrates. To aid biomonitoring and provide reference data for wildlife pesticide-risk assessment, plasma acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) activities were characterised in nine species of native bird: King Quails (Excalfactoria chinensis), Budgerigars (Melopsittacus undulatus), White-plumed Honeyeaters (Lichenostomas penicillatus), Yellow-throated Miners (Manorina flavigula), Willie Wagtails (Rhipidura leucophrys), Australian Reed-Warblers (Acrocephalus australis), Brown Songlarks (Cincloramphus cruralis), Double-barred Finches (Taeniopygia bichenovii) and Australasian Pipits (Anthus novaeseelandiae). Plasma ChE activities in all species were within the range of most other avian species and all but one contained AChE and BChE; no AChE was present in King Quail, which has not previously been reported for any species. The lowest detectable plasma AChE activity was 0.10 μmol min^–1 mL^–1 in Budgerigars and the highest was 0.86 μmol min^–1 mL^–1 in Australian Reed-Warblers. BChE in the plasma ranged from 0.37 μmol min^–1 mL^–1 in Double-barred Finches to 0.90 μmol min^–1 mL^–1 in White-plumed Honeyeaters and Australian Reed-Warblers. The lowest proportion of AChE was found in Budgerigars (12.8%) and highest in Willie Wagtails (67.8%). No differences were detected in ChE activity at any time of day in Budgerigars and Zebra Finches (Taeniopygia guttata), although there was a significant difference in all ChE activity between seasons in Zebra Finches.

The effect of acute fenitrotion exposure on a variety of physiological indices, including avian aerobic metabolism during exercise and cold exposure

The effect of fenitrothion exposure on birds was examined by measuring aerobic metabolism, blood hemoglobin content, plasma cholinesterases, and body weight for up to 21 d postdose. Peak metabolic rate was measured in a flight chamber in three-dose groups of house sparrows (Passer domesticus; 100 mg/kg = high, 60 mg/kg = medium, 30 mg/kg = low) and one-dose groups of zebra finches (Taeniopygia guttata; 3 mg/kg) and king quails (Coturnix chinensis; 26 mg/kg). Aerobic metabolism was measured during 1 h of exposure to subfreezing thermal conditions in low-dose house sparrows and king quails (26 mg/kg). Fenitrothion had no effect on metabolic rate during cold exposure or on blood hemoglobin at any time. By contrast, aerobic performance during exercise in sparrows was reduced by 58% (high), 18% (medium), and 20% (low), respectively, 2 d postdose. House sparrows (high) had the longest recovery period for peak metabolic rate (21 d) and plasma cholinesterase activity (14 d). House sparrows (high) and treated king quails had significantly lower myoglobin at 48 h postdose, whereas myoglobin was invariant in zebra finches and house sparrows (medium and low). Cholinesterase was maximally inhibited at 6 h postdose, and had recovered within 24 h, in house sparrows (low), king quails, and zebra finches. Exercise peak metabolic rate in zebra finches and king quails was reduced by 23% at 2 d and 3 d, respectively, despite these birds being asymptomatic in both behavior and plasma cholinesterase activities.

Cholinesterase response in native birds exposed to fenitrothion during locust control operations in Eastern Australia

Huge aggregations of flightless locust nymphs pose a serious threat to agriculture when they reach plague proportions but provide a very visible and nutritious resource for native birds. Locust outbreaks occur in spring and summer months in semiarid regions of Australia. Fenitrothion, an organophosphate pesticide, is sprayed aerially to control locust plagues. To evaluate fenitrothion exposure in birds attending locust outbreaks, we measured total plasma cholinesterase (ChE), butrylcholinesterase (BChE), and acetylcholinesterase (AChE) activities in four avian species captured pre- and postfenitrothion application and ChE reactivation in birds caught postspray only. Eleven of 21 plasma samples from four species had ChE activity below the diagnostic threshold (two standard deviations below the mean ChE activity of prespray samples). Granivorous zebra finches (Taeniopygia guttata) and insectivorous white-winged trillers (Lalage sueurii) had significantly lower mean plasma total ChE, BChE, and AChE activity postspray, while other insectivores, white-browed (Artamus superciliosus) and masked woodswallows (Artamus personatus), did not. Cholinesterase was reactivated in 19 of the 73 plasma samples and in one of three brain samples. We conclude that native bird species are exposed to fenitrothion during locust control operations. This exposure could have detrimental impacts, as both locust outbreaks and avian reproductive events are stimulated by heavy summer rainfall, leading to co-occurrence of locust control and avian breeding activities.

Developmental stress selectively affects the song control nucleus HVC in the zebra finch brain

Songbirds sing complex songs as a result of evolution through sexual selection. The evolution of such sexually selected traits requires genetic control, as well as selection on their expression. Song is controlled by a discrete neural pathway in the brain, and song complexity has been shown to correlate with the volume of specific song control nuclei. As such, the development of these nuclei, in particular the high vocal centre (HVC), is thought to be the mechanism controlling signal expression indicating male quality. We tested the hypothesis that early developmental stress selectively affects adult HVC size, compared with other brain nuclei. We did this by raising cross–fostered zebra finches (Taeniopygia guttata) under stressed and controlled conditions and determining the effect on adult HVC size. Our results confirm the strong influence of environmental conditions, particularly on HVC development, and therefore on the expression of complex songs. The results also show that both environmental and genetic factors affect the development of several brain nuclei, highlighting the developmental plasticity of the songbird brain. In all, these results explain how the complex song repertoires of songbirds can evolve as honest indicators of male quality.

Avian retinal oil droplets : dietary manipulation of colour vision?

Avian vision is highly developed, with bird retinas containing rod and double-cone photoreceptors, plus four classes of single cones subserving tetrachromatic colour vision. Cones contain an oil droplet, rich in carotenoid pigments (except VS/ultraviolet-sensitive cones), that acts as a filter, substantially modifying light detected by the photoreceptor. Using dietary manipulations, we tested the effects of carotenoid availability on oil droplet absorbance properties in two species: Platycercus elegans and Taeniopygia guttata. Using microspectrophotometry, we determined whether manipulations affected oil droplet carotenoid concentration and whether changes would alter colour discrimination ability. In both species, increases in carotenoid concentration were found in carotenoid-supplemented birds, but only in the double cones. Magnitudes of effects of manipulations were often dependent on retinal location. The study provides, to our knowledge, the first experimental evidence of dietary intake over a short time period affecting carotenoid concentration of retinal oil droplets. Moreover, the allocation of carotenoids to the retina by both species is such that the change potentially preserves the spectral tuning of colour vision. Our study generates new insights into retinal regulation of carotenoid concentration of oil droplets, an area about which very little is known, with implications for our understanding of trade-offs in carotenoid allocation in birds.