Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Does urbanization select for weak competitors in house sparrows?

How urbanization affects animal populations is in the focus of current ecological research. Existing theory of this topic suggests that the cities' more constant food supplies and lower predation pressure lead to a high proportion of weak competitors in urban populations. To evaluate this hypothesis, we tested whether competitive performance differs between differently urbanized populations of house sparrows Passer domesticus. We previously showed that wild urban sparrows are smaller and leaner than rural conspecifics, and this difference persists for months under identical captive conditions. Here we compared several aspects of their competitiveness (fighting, scrambling and searching for food) in captive mixed flocks of urban and rural birds. We found that sparrows exhibited consistent individual differences in competitiveness, but these differences were not related either to the degree of urbanization of their original habitats or to their body mass. Moreover, the variance in competitive abilities also did not differ between birds from more and less urbanized habitats. Thus our results did not support the hypothesis that urbanization shifts population structure towards an over‐abundance of weak competitors in house sparrows. We discuss possible explanations why sparrow populations may not differ in competitiveness despite the smaller body mass of urban birds.     

Effects of food shortage and oversupply on energy utilization, histology, and function of the gut in nestling song thrushes (Turdus philomelos)

We measured food intake, digestive efficiency, body mass increments, resting metabolic rate (RMR), carcass fat content, size and histological structure of the gut, and the rate of intestinal brush border uptake of l-proline in song thrush (Turdus philomelos) nestlings subjected to food shortage or food surplus under laboratory conditions. We assigned nestlings between 3 and 7 d of age to one of the following treatments: (1) food restriction, which resulted in a slowed growth at the rate found in undernourished, wild nestlings; (2) overfeeding, which totally suppressed begging; and (3) intermediate feeding. Threefold differences in energy consumption caused fivefold differences in body mass increments of the nestlings. Despite this, body mass-corrected RMR and intestinal mass were not affected by the feeding regime. The energy content of fecal output was highest in food-restricted birds, while their carcass fat content was lowest among treatment groups. Intestinal uptake rates of l-proline were low in the overfed and intermediate-fed young but significantly increased in the food-restricted birds, who attempted to maximize their rates of growth and development within the restrictive limits set by feeding regime. We noted a marked decrease of intestinal villi height in overfed birds as compared to intermediate-fed and food-restricted nestlings. We conclude that song thrush nestlings are characterized by a limited plasticity of their developmental program, which prohibits overfed nestlings from significantly up-regulating their gut function to accommodate increased food intake. This suggests that they already grew at a rate close to their physiological maximum. We suggest two interpretations: (1) under natural conditions, song thrush nestlings do not face frequent, unpredictable fluctuations in food abundance that could select for developmental plasticity, or (2) strong selection for uniform adult phenotypes prevents flexible developmental trajectories, which would result in a diversity of adult phenotypes.     

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'.     

Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning

Birdsong is a sexually selected trait and is often viewed as an indicator of male quality. The developmental stress hypothesis proposes a model by which song could be an indicator; the time during early development, when birds learn complex songs and/or local variants of song, is of rapid development and nutritional stress. Birds that cope best with this stress may better learn to produce the most effective songs. The developmental stress hypothesis predicts that early food restriction should impair development of song-control brain regions at the onset of song learning. We examined the effect of food restriction on song-control brain regions in fledgling (both sexes, 23-26 days old) song sparrows (Melospiza melodia). Food restriction selectively reduced HVC volume in both sexes. In addition, sex differences were evident in all three song-control regions. This study lends further support to a growing body of literature documenting a variety of behavioural, physiological and neural detriments in several songbird species resulting from early developmental stress.     

Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows

In seasonally breeding songbirds, brain nuclei of the song control system that act in song perception change in size between seasons. It has been hypothesized that seasonal regression of song nuclei may impair song discrimination. We tested this hypothesis in song sparrows (Melospiza melodia), a species in which males share song types with neighbors and must discriminate between similar songs in territorial interactions. We predicted that song sparrows with regressed song systems would have greater difficulty in discriminating between similar songs. Sparrows were housed either on short days (SD) and had regressed song circuits, or were exposed to long days and implanted with testosterone (LD+T) to induce full growth of the song circuits. We conducted two experiments using a GO/NO-GO operant conditioning paradigm to measure song discrimination ability of each group. Birds learned four (experiment 1) or three (experiment 2) pairs of song types sequentially, with each pair more similar in the number of shared song elements and thus more difficult to discriminate. Circulating T levels differed between the SD and LD+T groups. The telencephalic song nuclei HVc, RA, and area X were larger in the LD+T birds. The two groups of sparrows did not differ, however, in their ability to learn to discriminate between shared song types, regardless of the songs' similarity. These results suggest that seasonal changes in the song control system do not affect birds' ability to make difficult song discriminations.     

Spatial movements and social networks in juvenile male song sparrows

The time between fledging and breeding is a critical period in songbird ontogeny, but the behavior of young songbirds in the wild is relatively unstudied. The types of social relationships juveniles form with other individuals can provide insight into the process through which they learn complex behaviors crucial for survival, territory establishment, and mate attraction. We used radio telemetry to observe social associations of young male song sparrows (Melospiza melodia) from May to November. Juvenile song sparrows were frequently observed in social flocks and generally associated with more birds in the summer than in the autumn months. Most juvenile subjects formed stable social relationships with other birds and were seen with the same individual on up to 60% of the days observed. The strongest associations occurred with other juvenile males, and these individuals were often seen <1 m from the subject, even when the subject moved large distances between tracking observations. Associations also had long-term behavioral consequences as subjects were more likely to establish territories near their associates and learn shared song types. Our results indicate that male song sparrows spend a large percentage of the juvenile life stage forming social relationships and suggest that these associations may be important for the ecology of young birds and the ontogeny of their behaviors.     

Lean birds in the city: body size and condition of house sparrows along the urbanization gradient

1. Urbanized habitats differ from natural ones in several ecological features, including climate, food availability, strength of predation and competition. Although the effects of urbanization on avian community composition are well known, there is much less information about how individual birds are affected by these human-generated habitat differences. 2. In this study we investigated the relationships between the morphological characteristics and the degree of habitat urbanization in house sparrows, Passer domesticus (Linne 1758) . We collected data for more than 1000 non-breeding adult birds in Hungary between 1997 and 2006, from seven sites including farmlands, suburban areas and city centres. 3. We found that the body mass, tarsus length and body condition of free-living sparrows differed among the sites: birds in more urbanized habitats were consistently smaller and in worse condition than birds in more rural habitats. A composite measure of habitat urbanization (based on building density, road density and vegetation cover) explained over 75% of variance between sites in the studied traits, after we controlled for the effects of sex, year, season and time of capture. 4. The difference in body mass between rural and urban sparrows was significant when birds were kept in aviaries under identical conditions, with constant ad libitum food availability. It is therefore unlikely that the reduced body size and condition of urban sparrows are a consequence of reduced access to food for adults (e.g. due to strong competition), or their short-term responses to high food predictability (e.g. by strategic mass regulation). 5. We suggest that habitat differences in nestling development or adaptive divergence of sparrow populations due to distinct environmental conditions (such as differing predation pressure) may account for the differences along the urbanization gradient.     

Song Learning in Song Sparrows: Relative Importance of Autumn vs. Spring Tutoring

We examined ‘late’ song learning in song sparrows (Melospiza melodia), i.e., song learning that occurs after the first few months, or classical sensitive period, of the natal summer. Fledgling juveniles were brought into the laboratory at 2–3 mo of age and exposed to computer‐simulated song tutors in three different time periods: late in the natal summer, the autumn, and the next spring. As expected, the birds’ final repertoires consisted mostly of songs heard in the field, but 30% of the birds’ songs were influenced by songs heard in the laboratory (selective retention) and another 8% were learned de novo in the laboratory. Parallel results were obtained for a second group of birds who received laboratory tutoring only in the spring. In fact, the results suggested that autumn tutoring may even be inhibitory. We conclude that the songs a young song sparrow hears in his first spring may be critical to his final repertoire development, indicating that the song learning process in song sparrows is longer and more flexible than previously supposed.     

Trade-off between immune response and body mass in wintering house sparrows (<Emphasis Type="Italic">Passer domesticus</Emphasis>)

Immunity is necessary in order to fight parasites and pathogens, but immune protection also incurs a cost for the hosts. Therefore, immunity should be traded against other fitness-related traits. Body mass, as a function of body reserves, is important in birds of temperate zones during winter. Sedentary temperate birds usually increase body mass just before winter to survive a period with low food availability and thermoregulatory requirements. Given that immunity is costly and affects body mass, a trade-off is predicted between body mass and immunity in wintering birds. Such a trade-off was tested experimentally by stimulating the immune system of a group of wintering house sparrows (Passer domesticus) from a Spanish population in an outdoor aviary with a lipopolysaccharide while another group served as control. The activation of the immune system negatively affected body mass, despite the relatively mild temperatures of the study zone. Such a trade-off between body mass and immunity was found in other similar studies during breeding, but not during moult, suggesting that the trade-off between immunity and body mass may vary seasonally.     

3-Methylhistidine Excretion as an Index of Muscle Protein Breakdown in Birds in Different States of Malnutrition

Using 3-methylhistidine (3-MeHis) excretion as an index, we evaluated the abilities of molting and non-molting sparrows to adjust muscle protein degradation rates in response to three types of nutritional limitations: total food shortage, protein deficiency, or sulfur amino acid (SAA) deficiency. Regardless of nutritional status, molting birds excreted daily at least two-fold as much 3-MeHis as their non-molting counterparts. Both molting and non-molting birds significantly reduced daily excretion of 3-MeHis in response to a 1-day fast. Likewise, both molting and non-molting birds promptly reduced daily excretion of 3-MeHis in response to protein deficiency (within 1 day) and significantly so by day 5 and through day 9 of dietary treatment. Reductions in excretion of 3-MeHis by fasted or protein-limited birds could not be explained solely on the basis of reduced body protein mass and provided evidence of adjustments in muscle protein degradation rates. Responses of birds to SAA deficiency differed between molting and non-molting birds and from responses to the other nutritional limitations. In these birds, 3-MeHis excretion increased significantly on day 1 of dietary treatment. By day 5 and through day 9 of SAA deficiency, non-molting birds excreted 3-MeHis at rates similar to those of their well-nourished counterparts. In contrast, excretion of 3-MeHis by molting birds experiencing SAA deficiency remained significantly higher than by their well-nourished counterparts. Neither molting nor non-molting birds readily reduced muscle protein degradation rates in response to SAA deficiency and it is suggested that their failure to do so may provide evidence of a direct and (or) indirect role for glutathione in the regulation of muscle protein degradation.     

Living with the past: nutritional stress in juvenile males has immediate effects on their plumage ornaments and on adult attractiveness in zebra finches

The environmental conditions individuals experience during early development are well known to have fundamental effects on a variety of fitness-relevant traits. Although it is evident that the earliest developmental stages have large effects on fitness, other developmental stages, such as the period when secondary sexual characters develop, might also exert a profound effect on fitness components. Here we show experimentally in male zebra finches, Taeniopygia guttata, that nutritional conditions during this later period have immediate effects on male plumage ornaments and on their attractiveness as adults. Males that had received high quality food during the second month of life, a period when secondary sexual characteristics develop, were significantly more attractive as adults in mate choice tests than siblings supplied with standard food during this period. Preferred males that had experienced better nutritional conditions had larger orange cheek patches when nutritional treatments ended than did unpreferred males. Sexual plumage ornaments of young males thus are honest indicators of nutritional conditions during this period. The mate choice tests with adult birds indicate that nutritional conditions during the period of song learning, brain and gonad development, and moult into adult plumage have persisting effects on male attractiveness. This suggests that the developmental period following nutritional dependence from the parents is just as important in affecting adult attractiveness as are much earlier developmental periods. These findings thus contribute to understanding the origin and consequences of environmentally determined fitness components.     

THE INFLUENCE OF THE CALIFORNIA MARINE LAYER ON BILL SIZE IN A GENERALIST SONGBIRD

The hypothesis is tested that birds in hotter and drier environments may have larger bills to increase the surface area for heat dissipation. California provides a climatic gradient to test the influence of climate on bill size. Much of California experiences dry warm/hot summers and coastal areas experience cooler summers than interior localities. Based on measurements from 1488 museum skins, song sparrows showed increasing body‐size‐corrected bill surface area from the coast to the interior and declining in the far eastern desert. As predicted by Newton's convective heat transfer equation, relative bill size increased monotonically with temperature, and then decreased where average high temperatures exceed body temperature. Of the variables considered, distance from coast, average high summer temperature, and potential evapotranspiration showed a strong quadratic association with bill size and rainfall had a weaker negative relationship. Song sparrows on larger, warmer islands also had larger bills. A subsample of radiographed specimens showed that skeletal bill size is also correlated with temperature, demonstrating that bill size differences are not a result of variation in growth and wear of keratin. Combined with recent thermographic studies of heat loss in song sparrow bills, these results support the hypothesis that bill size in California song sparrows is selected for heat dissipation.     

Nestling growth and song repertoire size in great reed warblers: evidence for song learning as an indicator mechanism in mate choice

Females of many songbird species show a preference for mating with males that have larger song repertoires, but the advantages associated with this preference are uncertain. We tested the hypothesis that song complexity can serve as an indicator of male quality because the development of the brain regions underlying song learning and production occurs when young birds typically face nutritional and other stresses, so that song reflects how well a male fared during post-hatch development. A key prediction of this hypothesis is that variation in nestling condition should correspond to variation in the adult song repertoires of individuals. We used data from a long-term study of the great reed warbler (Acrocephalus arundinaceus) to test this prediction, correlating two measures of nestling development with subsequent repertoire size of males. We found that the length of the innermost primary feather, a standard measure of development, significantly predicted first-year repertoire size. The relationship between repertoire size and body mass was nearly significant, in spite of the large variance inherent in this measure. These data support the idea that song may provide females with information about a male's response to developmental stress, which in turn is expected to correlate with indirect or direct benefits she might receive.     

Early developmental stress negatively affects neuronal recruitment to avian song system nucleus HVC

Adverse environmental conditions can impact the life history trajectory of animals. Adaptive responses enable individuals to cope with unfavorable conditions, but altered metabolism and resource allocation can bear long‐term costs. In songbirds, early developmental stress can cause lifelong changes in learned song, a culturally transmitted trait, and nestlings experiencing developmental stress develop smaller song control nucleus HVCs. We investigated whether nutrition‐related developmental stress impacts neurogenesis in HVC, which may explain how poor nutrition leads to smaller HVC volume. We provided different quality diets (LOW and HIGH) by varying the husks‐to‐seeds ratio to zebra finch families for the first 35 days after the young hatched (PHD). At PHD14–18 and again at nutritional independence (PHD35), juveniles were injected with different cell division markers. To monitor growth, we took body measures at PHD10, 17, and 35. At PHD35 the number of newly recruited neurons in HVC and the rate of proliferation in the adjacent ventricular zone (VZ) were counted. Males raised on the LOW diet for their first weeks of life had significantly fewer new neurons in HVC than males raised on the HIGH diet. At the time when these new HVC neurons were born and labeled in the VZ (PHD17) the birds exposed to the LOW diet had significantly lower body mass. At PHD35 body mass or neuronal proliferation no longer differed. Our study shows that even transitory developmental stress can have negative consequences on the cellular processes underlying the development of neural circuits. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 107–118, 2016     

Carolina Chickadee (Aves, Paridae, Poecile carolinensis) Vocalization Rates: Effects of Body Mass and Food Availability under Aviary Conditions

We evaluated the effect of body mass and several environmental factors on vocalization rates of Carolina chickadees ( Poecile carolinensis ) housed in an aviary. Two different nonsong vocalizations (tseet and chick-a-dee) and song (fee-bee fee-bay) were recorded. Food was delivered from a feeder and three different levels of food access were presented to each bird: 10, 40 and 55 min/d. Two scales of body mass were measured: 'dawn mass' and 'focal mass' (mass during a focal observation divided by dawn mass). Across all birds, there was a significant negative correlation between both nonsong vocalization rates and body mass (both dawn and focal mass) and the effect of mass on call rate was greatest for days when food was relatively abundant. Nonsong vocalizations were also given at higher rates when food was limited (10 min/d) than when food was more abundant (40 and 55 min/d). No changes in call rates with time of day were observed. Overall, song rates were substantially lower than nonsong rates. Unlike nonsong rates, song rates were highest in birds that had relatively high dawn mass. No significant correlation between song rates and focal mass was observed, and no significant correlation between song rates and time of day was observed. Finally, vocalizations from nonfocal birds had little effect on vocalization rates of focal birds. Our results suggest that nonsong communicative signals are more important for birds facing energetic stress, while song is more important for birds that are not energetically stressed.     

Diet quality and food limitation affect the dynamics of body composition and digestive organs in a migratory songbird (Zonotrichia albicollis)

Migrating songbirds interrupt their feeding to fly between stopover sites that may vary appreciably in diet quality. We studied the effects of fasting and food restriction on body composition and digestive organs in a migratory songbird and how these effects interacted with diet quality to influence the rate of recovery of nutrient reserves. Food limitation caused white-throated sparrows to reduce both lean and fat reserves, with about 20% of the decline in lean mass represented by a decline in stomach, small intestine, and liver. During refeeding on diets similar in nutrient composition to either grain or fruit, food-limited grain-fed birds ate 40% more than did control birds, and they regained body mass, with on average 60% of the increase in body mass composed of lean mass including digestive organs. In contrast, food-limited fruit-fed birds did not eat more than did control birds and did not regain body mass, suggesting that a digestive constraint limited their food intake. The interacting effects of food limitation and diet quality on the dynamics of body composition and digestive organs in sparrows suggest that the adequacy of the diet at stopover sites can directly influence the rate of recovery of body reserves in migrating songbirds and hence the pace of their migration.     

Juvenile sparrows preferentially eavesdrop on adult song interactions

Recent research has demonstrated that bird song learning is influenced by social factors, but so far has been unable to isolate the particular social variables central to the learning process. Here we test the hypothesis that eavesdropping on singing interactions of adults is a key social event in song learning by birds. In a field experiment, we compared the response of juvenile male song sparrows (Melospiza melodia) to simulated adult counter-singing versus simulated solo singing. We used radio telemetry to follow the movements of each focal bird and assess his response to each playback trial. Juveniles approached the playback speakers when exposed to simulated interactive singing of two song sparrows, but not when exposed to simulated solo singing of a single song sparrow, which in fact they treated similar to heterospecific singing. Although the young birds approached simulated counter-singing, neither did they approach closely, nor did they vocalize themselves, suggesting that the primary function of approach was to permit eavesdropping on these singing interactions. These results indicate that during the prime song-learning phase, juvenile song sparrows are attracted to singing interactions between adults but not to singing by a single bird and suggest that singing interactions may be particularly powerful song-tutoring events.     

Sex-specific differences in compensation for poor neonatal nutrition in the zebra finch Taeniopygia guttata

Individuals can compensate for poor early nutrition by accelerating their growth rates once diet improves, but if malnutrition occurs at a key stage of development only certain body structures may compensate fully. This degrees of compensation is predicted to differ between the sexes and also between species with different life history strategies. In this paper we determine how males and females in a short-lived bird species, with only slight size dimorphism, differ in their abilities to compensate for a poor start in life. Here, zebra finch Taeniopygia guttata chicks from 93 broods were reared on either a standard quality (SQ), or low quality (LQ) diet for the first 15 d of life, followed by a standard diet for the rest of their lives. Thus, the period of nutritional manipulation was relatively short compared with previous studies. Nestlings on a LQ diet showed slower body mass and tarsus growth rates than those on SQ diet but this was reversed after the diet of the LQ birds was improved. LQ birds of both sexes were able to fully compensate in terms of body mass and beak colour, but not tarsus length. Body size and beak colour are sexually selected traits in male zebra finches. By adulthood LQ females had significantly shorter wings than other birds, apparently directing resources into sex-specific structures instead of feather and skeletal growth. Thus, our experiment showed that the sexes differed in how they phenotypically compensated for a poor start in life. Males in particular invested sparse resources into structures associated with mate acquisition, as proposed by life history theory for a species that 'lives fast and dies young.' We predict that this relatively short period of malnutrition during early development will have long term, sex-specific, fitness consequences for these birds.     

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds' bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting that the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.