Does testosterone mediate the trade-off between nestling begging and growth in the canary (Serinus canaria)?

Nestling birds solicit food from their parents with vigorous begging displays, involving posturing, jostling and calling. In some species, such as canaries, begging is especially costly because it causes a trade off against nestling growth. Fitness costs of begging like this are predicted by evolutionary theory because they function to resolve conflicts of interest within the family over the provision of parental investment. However, the mechanism that links these costs with nestling behaviour remains unclear. In the present study, we determine if the relationships between nestling androgen levels, nestling begging intensities and nestling growth rates are consistent with the hypothesis that testosterone is responsible for the trade-off between begging and growth. We test this idea with a correlational study, using fecal androgens as a non-invasive method for assaying nestling androgen levels. Our results show that fecal androgen levels are positively correlated with nestling begging intensity, and reveal marked family differences in each trait. Furthermore, changes in fecal androgen levels between 5 and 8 days after hatching are positively associated with changes in nestling begging intensity, and negatively associated with nestling growth during this time. Although these correlational results support our predictions, we suggest that that experimental manipulations are now required to test the direct or indirect role of testosterone in mediating the trade-off between begging and growth.

Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris).

Bird song is a sexually selected trait and females have been shown to prefer males that sing more complex songs. However, for repertoire size to be an honest signal of male quality it must be associated with some form of cost. This experiment investigates the effects of food restriction and social status during development on song complexity in the European starling (Sturnus vulgaris). Birds that experienced an unpredictable food supply early in life produced a significantly smaller repertoire of song phrases than those with a constant food supply. Social status during development was also significantly correlated with repertoire size, with dominant birds producing more phrase types. This study therefore provides novel evidence that social as well as nutritional history may be important in shaping the song signal in this species.

Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata).

In a wide range of bird species, females have been shown to express active preferences for males that sing more complex songs. Current sexual selection theory predicts that for this signal to remain an honest indicator of male quality, it must be associated with an underlying cost of development or maintenance. There has been considerable debate questioning the costs associated with song production and learning. Recently, the nutritional stress hypothesis proposed that song complexity could act as an indicator of early developmental history, since the song control nuclei in the brain are laid down early in life. Here we test the nutritional stress hypothesis, by investigating the effects of dietary stress on the quality of adult song produced. In addition, we tested the effects of elevated corticosterone during development on song production to test its possible involvement in mediating the effects of developmental stress. The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates. In addition, we found that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity. These results provide novel experimental evidence that complex song repertoires may have evolved as honest signals of male quality, by indicating early developmental rearing conditions.

Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris).

Bird song is a sexually selected male trait where females select males on the basis of song quality. It has recently been suggested that the quality of the adult male song may be determined by nutritional stress during early development. Here, we test the 'nutritional-stress hypothesis' using the complex song of the European starling. Fledgling starlings were kept under experimental treatment (unpredictable short-term food deprivations) or control conditions (ad libitum food supply), for three months immediately after independence. We measured their physiological and immune responses during the treatment and recorded song production during the following spring. Birds in the experimental group showed increased mass during the treatment and also a significantly suppressed humoral response compared with birds in the control group. There was no difference between the groups in the cell-mediated response. Next spring, males in the experimental group spent less time singing, sang fewer song bouts, took longer to start singing and also sang significantly shorter song bouts. These data support the hypothesis that both the quality and quantity of song produced by individual birds reflect past developmental stress. The results also suggest the 'nutritional-stress hypothesis' is best considered as a more general 'developmental-stress hypothesis'.

The influence of flicker rate on plasma corticosterone levels of European starlings, Sturnus vulgaris.

Recent reviews have highlighted the differences between human and avian vision with regard to temporal resolution and the potential problems it may cause for avian welfare and video playback experiments. Birds tend to have much higher critical fusion frequencies than do humans (>100 Hz vs 50-60 Hz in humans), which means that they perceive light as flickering up to and over 100 Hz. This is higher than most television monitors (which have refresh rates of 50 or 60 Hz) and normal fluorescent lighting (100 or 120 Hz), and because humans find flickering light aversive, it has been suggested that birds will as well. If this were the case, then there would be welfare implications of maintaining them under such lighting and also a potential effect on their behavioral responses in video playback experiments. However, there is some behavioral evidence that indicates that birds do not appear to find flicker aversive and may even prefer flickering lighting. The authors aimed to determine whether a passerine, the European starling, found flicker aversive by measuring the corticosterone stress response in birds maintained under high- or low-frequency fluorescent lighting (35-40 kHz vs 100 Hz) for 1 or 24 h. The results suggest that low-frequency lighting is potentially more stressful because, where differences exist, birds in the low-frequency treatment always showed higher basal corticosterone. However, the evidence is not consistent because in half of the blocks, there were no significant treatment effects and, where there were, the time course of the effects was variable.

Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling?

Sexually selected signals of individual dominance have profound effects on access to resources, mate choice and gene flow. However, why such signals should honestly reflect individual quality is poorly understood. Many such signals are known to develop under the influence of testosterone. We conducted an experiment in male house sparrows in which testosterone was manipulated independently during two periods: before the onset of the breeding season and prior to the autumn moult. We then measured the effects of these manipulations on basal metabolic rate and on the size of the chest bib, a sexually selected signal. The results demonstrate that testosterone simultaneously affects both signal development and basal metabolic rate in the house sparrow (Passer domesticus). This evidence, therefore, supports a novel conclusion: that testosterone-dependent signals act as honest indicators of male quality possibly because only high-quality individuals can sustain the energetic costs associated with signal development.

Lack of gonadotrophin-releasing hormone (GnRH) neuron response to decreasing photoperiod in thyroidectomized male starlings (Sturnus vulgaris).

Exposure of starlings to long days initially causes reproductive maturation, but eventually leads to photorefractoriness. During photorefractoriness, gonadotrophin-releasing hormone (GnRH) decreases in the GnRH cell bodies and fibers emanating from these to the median eminence, circulating gonadotrophin concentrations decrease to a minimum, and the gonads regress. Thyroidectomy profoundly affects these photoperiodic responses. In chronically thyroidectomized starlings, gonadal responses to changes in day length are attenuated. This investigation was conducted to determine whether, in the absence of gonadal responsiveness, the GnRH system of chronically thyroidectomized starlings responds to changes in day length. Two groups of thyroidectomized male starlings were transferred from short days (8L:16D) to long days (18L:6D) for four weeks, and testicular volume increased. One group was kept on long days (TxLD) and the other was returned to short days (TxSD). Testicular volume did not decrease in the TxSD group. The GnRH neurons of the two thyroidectomized groups were compared to those of two groups of intact starlings, one of them on long days and photorefractory (ILD), the other on short days and photosensitive (ISD). Group ILD had lower numbers of GnRH-stained cells than groups TxLD, TxSD and ISD, which did not differ in this respect. Similar differences were observed for GnRH cell size in the pre-optic area (POA) and for density of staining of GnRH fibers in the median eminence. The results confirm that thyroidectomy attenuates gonadal responses to change in day length and suggest that this results from an effect upon the central nervous system rather than a peripheral effect.

Decreased light intensity alters the perception of day length by male European starlings (Sturnus vulgaris).

The breeding season of wild starlings is controlled by photoperiod. Full breeding condition is attained during exposure to lengthening days in the spring, and photorefractoriness ensues. The reproductive system of starlings will not subsequently be stimulated by long day lengths until photorefractoriness is dissipated by the short day lengths experienced in the autumn and winter. Unlike most studies on avian photoperiodism, this investigation involved manipulation of light intensity of a fixed photoperiod rather than of photoperiod itself. Photosensitive starlings transferred from short days to long days of different light intensities underwent graded reproductive responses according to the light intensity they experienced. Testes size in the group in the lowest intensity (3 lux) increased faster than that in controls on short days of normal intensity, but they did not become photorefractory. Testes size increased in the groups on 13, 45, and 108 lux and subsequently became photorefractory. However, the 13- and 45-lux groups required more time to become photorefractory than did the 108-lux group. The responses observed were similar to those seen in starlings exposed to different photoperiods (e.g., 11 h light:13 h dark [11L:13D], 13L:11D, 16L:8D, 18L:6D), even though all were on the same 18L:6D photoperiod. Initially, the results appear to challenge the external coincidence model for photoperiodic time measurement, but consideration of the phase response curve of the circadian rhythm of photoinducibility in starlings and the way in which it might be affected by low light intensities refute this challenge.

Changes in gonadotrophin-releasing hormone (GnRH-I) in the pre-optic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation.

Changes in GnRH-I in the pre-optic (POA) and medio-basal (MBH) areas of the hypothalamus and in pituitary and plasma LH were measured in starlings (Sturnus vulgaris) during the recovery of photosensitivity under short days, and following photostimulation at various times during the recovery of photosensitivity. During exposure to short days there was a significant increase in GnRH-I in the POA, with the first detectable increase after only 10 days. There was no increase in GnRH-I in the MBH or in pituitary or plasma LH. In birds photostimulated after 10 short days, there was an increase in GnRH-I in the POA, but this was no greater than that in birds remaining under short days. There was no increase in GnRH-I in the MBH or in plasma LH. Photostimulation after 20 short days caused an immediate increase in GnRH-I in the POA, delayed increase in GnRH-I in the MBH, but no increase in plasma LH. Photostimulation after 30 short days caused an immediate increase in GNRH-I in the POA and the MBH and in plasma LH. The results show that the recovery of photosensitivity is gradual; the first measurable change occurs in the POA, consistent with photosensitivity being due to renewed GnRH-I synthesis. The effects of photostimulation increase, both in magnitude and in terms of how far 'downstream' of the POA changes are apparent, as photosensitivity is gradually restored. The results support the hypothesis that daylength has a dual role, controlling both synthesis and secretion of GnRH.

Photorefractoriness in European starlings (Sturnus vulgaris) is not dependent upon the long-day-induced rise in plasma thyroxine.

Transfer of intact, photosensitive starlings from short to long days causes an increase in plasma thyroxine and gonadal maturation and later induces photorefractoriness. Thyroidectomy of starlings prevents the induction of photorefractoriness. This study investigated whether the long-day-induced increase in plasma thyroxine is necessary for the induction of photorefractoriness. Photosensitive starlings were thyroidectomised, given thyroxine in their drinking water at concentrations that result in plasma thyroxine at short-day physiological concentrations or lower, and transferred to long days. Plasma thyroxine and prolactin, gonadal size, and moult were monitored. The group with short-day concentrations of plasma thyroxine became photorefractory at the same time as intact controls transferred to long days. The other groups, with lower plasma thyroxine, also became photorefractory, but the onset of photorefractoriness was delayed. The increase in plasma prolactin following photostimulation was proportional to plasma thyroxine concentrations. The onset of moult was also related to plasma thyroxine. We conclude that the long-day concentrations of plasma thyroxine observed in the plasma of intact starlings are not necessary for the induction of photorefractoriness. This suggests that thyroxine acts as a permissive factor rather than actively driving the photorefractory process.

The effects of nerve growth factor and anti-nerve growth factor antibody on the neuroendocrine reproductive system in the European starling Sturnus vulgaris.

Thyroidectomy of starlings causes them to remain in breeding condition indefinitely; deactivation of gonadotrophin-releasing hormone neurons that is characteristic of photorefractoriness does not occur. We hypothesise that a neurotrophin, whose presence or ability to function is dependent upon thyroid hormones, is somehow involved in this termination of gonadotrophin-releasing hormone release. Nerve growth factor is one such candidate. Mouse 7S-nerve growth factor dissolved in artificial cerebro-spinal fluid was therefore infused into the lateral ventricle of thyroidectomised male starlings held on long days four times daily for 21 days and 31 days, in separate experiments, to see if photorefractoriness would occur. The result was significant gonadal regression in the treatment groups during the infusion period, with no change in testicular volume in the control groups. Testicular recrudescence occurred after the end of the treatment period. To see if this was a non-specific effect, or progression towards photorefractoriness per se, we used castrated, photorefractory starlings held on long days. Anti-nerve growth factor antibody was infused into the lateral ventricle at increasing concentrations and frequency. There was a significant rise in circulating luteinising hormone levels in the treatment groups as compared to controls, increasing with antibody dosage.

Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness.

Immunocytochemistry with quantitative image analysis, for both GnRH and its precursor proGnRH-GAP, was used in male European starlings (Sturnus vulgaris) to investigate four stages of a photoperiodically-induced reproductive cycle. Four different groups of birds were examined: photosensitive buy sexually immature, sexually mature, undergoing gonadal regression, and after the completion of regression and fully photorefractory. The size of cells staining for GnRH and proGnRH-GAP increased during gonadal maturation. A reduction in the number of cells staining for GnRH and the size of cells staining for both GnRH and proGnRH-GAP occurred during gonadal regression, though staining for GnRH and proGnRH-GAP in the median eminence remained high at this stage. Birds examined after completion of regression showed significantly reduced staining for both GnRH and its precursor. These observations suggest that photorefractoriness is promoted by a reduction in proGnRH-GAP production and in GnRH synthesis, rather than requiring inhibition of release of GnRH at the median eminence.

Migratory fat deposition in European quail: a role for prolactin?

The present study addresses the role of prolactin as a regulator of migratory fattening in European quail (Coturnix coturnix). Plasma prolactin levels in captive birds undergoing migratory fattening in an outdoor aviary and in the laboratory were measured by radioimmunoassay with an antibody raised against recombinant-derived chicken prolactin. No strong association between prolactin and migratory fattening was apparent, and prolactin levels were more closely related to daylength, with the highest concentrations being reached on long days. Plasma prolactin profiles were similar in intact and castrated male quail. Prolactin was secreted in a daily rhythm, with the highest concentrations occurring early in the photophase. However, when birds were food-restricted for 50 days during a migratory phase, there was no difference in fat deposition between birds food-deprived for the first half of the daily photophase compared with those deprived for the second half. Fattening was reduced in the food-restricted birds relative to ad libitum-fed controls, but there was no difference in plasma prolactin levels between the groups. Injections of ovine prolactin (4 mg/kg) significantly increased food intake and body mass of birds maintained on long days, but there were no differences in fattening between birds injected in the morning compared with those injected in the afternoon. Collectively, these results do not support a major role for prolactin in the regulation of migratory fat deposition in European quail.

The effect of duration of exposure to short days on the gonadal response to long days in male starlings (Sturnus vulgaris).

Photorefractory male starlings (Sturnus vulgaris) were transferred from a photoperiodic schedule of 18 h light:6 h dark to 8 h light:16 h dark for 2, 4, 6 or 10 weeks, and then photostimulated by exposure to 18 h light:6 h dark. Testicular dimensions were measured at regular intervals by laparotomy. There was no change in testicular volume in birds photostimulated after 2 weeks under a photoperiod of 8 h light:16 h dark, but a cycle of testicular growth followed by regression occurred in the other groups. Testicular volume was increased significantly by 20 days under 18 h light:6 h dark in all three groups; regression began after 45, 65 and 75 days in birds pre-exposed to 8 h light:16 h dark for 4, 6 and 10 weeks, respectively. These results are discussed in relation to other evidence for the progressive development of photosensitivity.

A comparison of the responses to gonadotrophin-releasing hormone of adult and juvenile, and photosensitive and photorefractory European starlings, Sturnus vulgaris.

The reproductive system of juvenile European starlings appears to be similar to that of photorefractory adults, yet the increase in plasma luteinizing hormone (LH) in juveniles in response to gonadotrophin-releasing hormone (GnRH) is much less than that of photorefractory adults. To investigate this apparent anomaly, the effects of age, reproductive state, and sex on the increase in plasma LH concentration in response to im injections of GnRH were investigated. The results show that photorefractory juveniles needed 10 times the dose of GnRH to elicit the same increase in LH as photorefractory adults, and the response of photosensitive juveniles to 10 micrograms GnRH was at least 15 times as great as that of photorefractory juveniles (e.g., 6.14 micrograms/liter compared to 0.35 microgram/liter 2 min after injection). However, the response of photosensitive adults was not greater than that of photorefractory adults. These differences were not due to differences in the amount of LH stored in the pituitary: this was 298 +/- 34 and 306 +/- 51 ng/gland in photorefractory juveniles and adults, respectively, and 367 +/- 47 in photosensitive juveniles. Repeated weekly treatment with GnRH enhanced LH responses: LH levels 3 min after GnRH treatment increased in birds on short days from 7.7 micrograms/liter after the first treatment to 24.6 micrograms/liter after the sixth treatment and in birds on long days it increased from 0.54 to 1.8 micrograms/liter. The greater response of photorefractory adults compared to photorefractory juveniles may therefore be due to the self-priming effect of GnRH during a preceding period of photosensitivity and/or photostimulation. The response to exogenous GnRH depends more on age and history than on prevailing physiological state. There was also a marked sex difference: females showed a sevenfold greater response to GnRH.

Acquisition of photosensitivity in castrated male starlings (Sturnus vulgaris) under short day photoperiods.

Photorefractory castrated male starlings were transferred from a photoperiodic schedule of 18 h light:6 h dark to 1 h light:23 h dark, 5 h light:19 h dark, 8 h light: 16 h dark or 11 h light:13 h dark. Plasma concentrations of LH were measured in blood samples taken at regular intervals, to give an indication of the reacquisition of photosensitivity under these schedules. Concentration of plasma LH increased after 35, 38, 35 and 63 days, respectively; there was a steady increase in LH in all groups, but the increase under 11 h light:13 h dark was much slower than in the other groups. In contrast, birds held under 18 h light:6 h dark showed no increase in LH. Thus, starlings became photosensitive at a similar rate under fixed photoperiods of 8 h light:16 h dark or shorter, but took longer to acquire photosensitivity under 11 h light:13 h dark.

Ultrastructural evidence for changes in synaptic input to the hypothalamic luteinizing hormone-releasing hormone neurons in photosensitive and photorefractory starlings.

Neural input to the hypothalamic luteinizing hormone-releasing hormone (LHRH) neurons was investigated in male starlings (Sturnus vulgaris) using electron microscopy combined with immunocytochemistry. Birds (4 to 6 in each group) were sampled at four stages of a photoperiodically induced reproductive cycle: (a) sexually immature but photosensitive, under short days; (b) during sexual maturation after 7 to 25 long days; (c) during gonadal regression after 35 to 50 long days; and (d) when fully photorefractory after 11 months exposure to long days. The length of the perikaryal membrane, the number and length of axo-somatic terminals in contact with it and the number and length of synaptic modifications within the terminals were measured for a minimum of six LHRH neurons in each brain. The number of axo-somatic terminals per neuron and the number per unit length of perikaryal membrane did not differ in birds of groups (a), (b) and (c), but was significantly greater (P < 0.05) in the fully refractory birds (group d). Similarly, the number of synaptic modifications was significantly greater (P < 0.05) in group (d) than in the other groups. These results are consistent with increased neural input to the LHRH perikarya in photorefractory birds after prolonged exposure to long days, although there was no indication of a change in input at the time of gonadal regression.

Prolactin and gonadal steroids during the reproductive cycle of the Bengalese finch (Lonchura striata var. domestica, Estrildidae), a nonseasonal breeder with biparental care.

Plasma levels of prolactin (Prl), testosterone (T), and progesterone were determined throughout the breeding cycle in pairwise caged Bengalese finches (Lonchura striata var. domestica, Estrildidae), a monogamous altricial passerine with nonseasonal breeding, in which parental behavior including incubation is equally shared between males and females. In both sexes, Prl titers increased 4- to 10-fold during incubation period compared to values during nestbuilding. Likewise, Prl levels after fledging of the young were significantly lower compared to titers during incubation. In males, T increased significantly (15-fold) during nestbuilding compared to all other stages of the breeding cycle. In females, T remained basal throughout the entire breeding cycle. Thus, T levels were elevated only during stages with low Prl titers and vice versa. Progesterone titers were elevated during egg-laying in females and fluctuated without any obvious pattern in males. These results suggest that (1) high levels of Prl are involved in the control of parental behavior of male and female Bengalese finches and (2) Prl secretion is controlled by proximate factors of the early reproductive cycle since reproduction is independent of seasonal factors in this species.

Puberty in birds: the reproductive system of starlings does not respond to short days until birds are fully grown.

If adult starlings are kept on long days, they rapidly become refractory to long days (photorefractory). The recovery of the ability to respond to long days (photosensitivity) occurs after transfer to short days. Photosensitivity is associated with an increase in hypothalamic content of gonadotrophin-releasing hormone (GnRH), and, in castrated birds, with an increase in plasma LH. If photorefractory adult or juvenile starlings are transferred to short days, these events begin 3 and 4 weeks respectively after transfer. Starlings apparently hatch in a photorefractory state. However, if nestlings are hand-reared under short days, the increases in GnRH and LH begin at 6 and 7 weeks of age respectively. In this 3-week delay, which corresponds to the time to reach adult body size, simply due to a slower response, or are nestlings incapable of responding to short days until fully grown? Castrated male nestling starlings were hand-reared under short days, under long days or under long days initially and transferred to short days at 2, 3, 6 or 9.5 weeks of age. The increase in plasma LH in birds transferred to short days at or before 3 weeks began at the same time as in birds kept on short days (7 weeks). In birds transferred at 3 weeks or later, the increase in LH began 4 weeks after transfer, irrespective of age. Intact female starlings showed similar responses. Birds kept on short days did not moult whereas birds transferred from long days to short days at 3 weeks did.(ABSTRACT TRUNCATED AT 250 WORDS)

Thyroxine treatment induces changes in hypothalamic gonadotrophin-releasing hormone characteristic of photorefractoriness in starlings (Sturnus vulgaris).

Photosensitive intact male starlings were transferred from short days (8L:16D) to 11L:13D for 16 weeks, and were therefore sexually mature. Experimental groups were (i) held under 11L:13D and given exogenous thyroxine dissolved in the drinking water for 6 weeks or (ii) given thyroxine for 6 weeks and then transferred from 11L:13D to long days (18L:6D) for a further 6 weeks, while control groups were transferred to long days (18L:6D) either (iii) for 6 or (iv) for 12 weeks, or were (v) maintained under 11L:13D throughout. Changes in testicular size and plumage molt were monitored at regular intervals during the 12-week period. At the end of the experiment, the birds were killed and hypothalamic gonadotropin-releasing hormone (Gn-RH) content and testicular mass were measured. Treatment with exogenous thyroxine caused rapid testicular regression followed by plumage molt, and after 6 weeks hypothalamic Gn-RH content was much reduced, to an even greater extent than that in control birds exposed to long days for 6 weeks. After 6 weeks of thyroxine treatment, withdrawal of exogenous thyroxine and exposure to long days for a further 6 weeks caused no increase in testicular size, and caused a further reduction in hypothalamic Gn-RH content to a level similar to that in controls after 12 weeks of exposure to long days. The results confirm previous findings that thyroxine induces a state of photorefractoriness in sexually mature starlings and show for the first time that the treatment mimics the effect of long days in reducing Gn-RH content in the hypothalamus.