A recipe for postfledging survival in great tits Parus major: be large and be early (but not too much)

Survival of juveniles during the postfledging period can be markedly low, which may have major consequences on avian population dynamics. Knowing which factors operating during the nesting phase affect postfledging survival is crucial to understand avian breeding strategies. We aimed to obtain a robust set of predictors of postfledging local survival using the great tit (Parus major) as a model species. We used mark–recapture models to analyze the effect of hatching date, temperatures experienced during the nestling period, fledging size and body mass on first‐year postfledging survival probability of great tit juveniles. We used data from 5192 nestlings of first clutches ringed between 1993 and 2010. Mean first‐year postfledging survival probability was 15.2%, and it was lower for smaller individuals, as well as for those born in either very early or late broods. Our results stress the importance of choosing an optimum hatching period, and raising large chicks to increase first‐year local survival probability in the studied population.     

Is cell-mediated immunity related to the evolution of life-history strategies in birds?

According to life-history theory, the development of immune function should be balanced through evolutionary optimization of the allocation of resources to reproduction and through mechanisms that promote survival. We investigated interspecific variability in cell-mediated immune response (CMI), as measured by the phytohaemagglutinin (PHA) assay, in relation to clutch size, longevity and other life-history traits in 50 species of birds. CMI exhibited significant repeatability within species, and PHA responses in chicks were consistently stronger than in adults. Univariate tests showed a variety of significant relationships between the CMI of both chicks and adults with respect to size, development period and lifespan, but not clutch size or prevalence of blood parasites in adults. Multivariate analyses confirmed these patterns but independent variables were too highly correlated to isolate unique influences on CMI. The positive relationship of chick CMI to nestling period is further complicated by a parallel relationship of chick CMI to the age at testing. However, multivariate analysis showed that chick CMI varies uniquely with length of the nestling period. Adult CMI was associated with a strong life-history axis of body size, development rate and longevity. Therefore, adult CMI may be associated with prevention and repair mechanisms related to long lifespan, but it also may be allometrically related to body size through other pathways. Neither chick CMI nor adult CMI was related to clutch size, contradicting previous results linking parasite-related mortality to CMI and the evolution of clutch size (reproductive investment) in birds.     

Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica)

Laying date is one of the most important determinants of reproductive success and recruitment probability in birds. Late breeders usually fledge fewer chicks than individuals with earlier breeding dates, and fledglings produced late in the season have high mortality rates. Food availability and nestling mass have been evoked as the principal mechanistic links between laying date and offspring survival. Here we suggest that another factor may actually account for the difference in survival rate between early and late offspring: immunocompetence. We predicted that nestlings produced later in the season or in replacement clutches should have lower immune responses when challenged with an antigen, than early nestlings or nestlings produced in first clutches. This hypothesis was tested in a population of magpies (Pica pica), in which we experimentally induced breeding failure in a group of nests and compared the immune response of nestlings in replacement clutches with the immune response of first clutch nestlings. Cellular immune response, as measured by wing web swelling (a correlate of T-lymphocyte production after injection of phytohaemagglutinin-P), significantly decreased with hatching date and was significantly lower in nestlings of replacement clutches. Furthermore, coefficients of intraclutch variation in immune response were higher in nestlings of replacement clutches. This experiment demonstrates an inverse relationship between immune responsiveness and breeding date, and reduced recruitment probability of late nestlings may be a direct consequence of their inability to cope with parasites.     

Decline of a montane Mediterranean pied flycatcher Ficedula hypoleuca population in relation to climate

Certain populations of long‐distance migratory birds are suffering declines, which may be attributed to effects of climate change. In this article, we have analysed a long‐term (1991–2015) data set on a pied flycatcher Ficedula hypoleuca population breeding in nest‐boxes in a Mediterranean montane oak forest, exploring the trends in population size due to changes in nestling recruitment, female survival and female immigration. We have related these changes in population parameters to local climate, winter NAO index and to breeding density. During the last 25 yr the population has declined by half, mainly in association with a decrease in nestling mass and structural size which had repercussions on the probability of nestling recruitment to the population. Lower local nestling recruitment in certain years was linked to lower female immigration rate in the same years. On the other hand, the local survival of females remained stable throughout the study period. Laying date and breeding success were negatively affected by local temperatures while breeding, recruitment rate likewise by minimum temperature prior to breeding in April. As minimum April temperatures have increased across the study period, this may have affected recruitment and immigration rates negatively. On the other hand, tarsus length and body mass of nestlings were positively associated with winter NAO index, pointing to more global climatic links. Moreover, there was also a negative temporal trend in body mass of adults, implying increasingly difficult conditions for breeding. Declining recruit production in the study area could be attributed to a mismatch between the timing of arrival and breeding in the population, and the peak of food availability in this area.     

Juvenile survival and recruitment of wood thrushes Hylocichla mustelina in a forest fragment

We tested if juvenile survival and recruitment (returning to breed) of wood thrushes Hylocichla mustelina into their natal population was dependent on several measures of nestling condition, growth, and site fidelity. Overall, nestling mass, wing chord, condition, and rank within the brood did not affect the probability of survival to the post-fledging stage, independence, or recruitment. We did not identify any morphometric differences among nestlings that remained in the study area after fledging and those that did not (or those that did not survive). Time of season and the number of days nestlings were present in the study area after hatching, or site fidelity, were the only variables measured that positively influenced juvenile survival and recruitment. Based on a restricted sample, fledglings that eventually recruited did not differ in size during post-fledging or post-independence from fledglings that did not return to breed. Independent, immigrant hatching-year (HY) birds are briefly described. Overall, immigrant HY birds had a higher probability of recruitment than all local fledglings. There was no difference in the probability of recruitment between immigrant HY birds and independent local fledglings (those present ≥35 days after hatching), however. Similar to local young, the number of days present in the study area increased the likelihood of recruitment for immigrant HY birds, although these effects could not be distinguished from those of emigration or survival.     

Correlates of cell-mediated immunity in nestling house sparrows

Cell-mediated immunity is an important vertebrate defense against pathogens, but components of this response may vary in quality. Such variation could arise through the effects of ecology on optimal immunocompetence. We used injections of phytohaemagglutinin (PHA) to measure the factors influencing T-cell proliferation in nestling house sparrows (Passer domesticus). Bivariate analyses revealed positive associations with nestling mass and size, but no effect of ectoparasites. The response to PHA was, however, strongly affected by brood identity. A mixed model with brood identity as a random factor and nestling mass, size, number of ectoparasites, parental feeding rate, clutch size, brood size at hatching, and date uncovered significant positive correlations between PHA response and both nestling mass and the brood size at hatching. Because many of these variables are related hierarchically, we used path analysis to explore the relationships in more detail. We found that a nestling immune response was affected by several indirect paths. Brood size at hatch had both positive and negative paths, and date in the season had several indirect negative effects through its effect on brood size and nestling mass. The approach used and the results obtained offer some new ideas for incorporating immune responses into life history theory.     

Hatching asynchrony and brood reduction influence immune response in Common Kestrel Falco tinnunculus nestlings

The onset of incubation before the end of laying imposes asynchrony at hatching and, therefore, a size hierarchy in the brood. It has been argued that hatching asynchrony might be a strategy to improve reproductive output in terms of quality or quantity of offspring. However, little is known about the mediating effect of hatching asynchrony on offspring quality when brood reduction occurs. Here, we investigate the relationship between phenotypic quality and hatching asynchrony in Common Kestrel Falco tinnunculus nestlings in Spain. Hatching asynchrony did not increase breeding success or nestling quality. Furthermore, hatching asynchrony and brood reduction had different effects on nestlings’ phytohaematogglutinin (PHA)‐mediated immune response and nestling growth. In asynchronous and reduced broods (in which at least one nestling died), nestlings showed a stronger PHA‐mediated immune response and tended to have a smaller body size compared with nestlings raised in synchronous and reduced broods. When brood reduction occurred in broods hatched synchronously, there was no effect on nestling size, but nestlings had a relatively poor PHA‐mediated immune response compared with nestlings raised in asynchronous and reduced broods. We suggest that resources for growth can be directed to immune function only in asynchronously hatched broods, resulting in improved nestling quality, as suggested by their immune response. We also found that males produced a greater PHA‐mediated immune response than females only in brood‐reduced nests without any effect on nestling size or condition, suggesting that females may trade off immune activities and body condition, size or weight. Overall, our results suggest that hatching pattern and brood reduction may mediate resource allocation to different fitness traits. They also highlight that the resolution of immune‐related trade‐offs when brood reduction occurs may differ between male and female nestlings.     

Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings

Diversity of the gut bacterial community is of prime importance for optimal food digestion and, therefore, for nutritional condition of avian nestlings. Consequently, bacterial community should be considered as a predictor of the future survival and recruitment of young birds. To explore this hypothesis, we studied the cloacal microbiota, by using RISA procedure, in two avian species sharing environmental conditions during growth, the avian brood parasitic great spotted cuckoo Clamator glandarius , and their main host in Europe, the magpie Pica pica . As estimates of phenotypic condition of nestlings we studied two nutrition-dependent traits, the immune response to an innocuous antigen (phytohemagglutinin), and the residuals of body mass on tarsus and wing length of nestlings. According to the hypothesis, we found significant relationships between microbial diversity and nestling phenotypic traits related to probability of recruitment. Briefly, both magpie and cuckoo nestlings having more similar microbial diversity were also those with similar immune response and body condition index respectively. Our results show a possible association between bacterial communities and variables related to the probability of post-fledging survival and recruitment of birds, as well as possible reasons explaining magpie-cuckoo differences in the nutritionally conditioned variables better associated with their bacterial diversity.     

Immune function and survival of great tit nestlings in relation to growth conditions

Life history theory predicts a trade-off between number and quality of offspring. Reduced quality with increasing brood size may arise from a decrease in body condition or in immunocompetence that would be important in fighting off virulent parasites by immunologically naive offspring. We tested the effect of rearing conditions on immune function of nestling great tits (Parus major) by reducing or increasing broods by two hatchlings. In the middle of the nestling period (on day 8), nestlings from enlarged broods developed lower T cell responses [as measured from the cutaneous swelling reaction to injection with phytohaemagglutinin (PHA)] and tended to have lower total leukocyte and lymphocyte concentrations in their peripheral blood than nestlings from reduced broods. Brood size manipulation affected the PHA response of nestlings most strongly in small clutches, suggesting that nestling immune function was dependent on their parents’ condition, as estimated by original clutch size. Intra-brood differences in nestling mortality were unrelated to immune parameters, but nestlings in broods without mortality had a stronger PHA response, higher concentration of lymphocytes and higher body mass on day 15 than nestlings in broods with mortality. These results support the prediction that the immune function of altricial birds is affected by rearing conditions, and that growth and immune parameters are related to inter-brood differences in nestling survival. Received: 1 February 1999 / Accepted: 19. July 1999     

Cell-mediated immunity predicts the probability of local recruitment in nestling blue tits

We investigated whether the variation in T-cell-mediated immune function of blue tit nestlings affected their fledgling success and the probability of local survival. We studied the relationship between immune function and survival under two rearing conditions: control, unmanipulated, and experimentally enlarged broods. Brood enlargement had negative effects on nestling immune response. Immune response was positively related to fledgling success and it predicted the probability of local recruitment. However, the relationship between immune response and the probability of recruitment was significantly positive only among control broods and nonsignificant among enlarged broods. The effect of immune response on the recruitment probability was not affected by variation in body mass. Our study suggests that selection for immune responsiveness seems to be weak or even absent under unfavourable rearing conditions as simulated by brood size enlargement. Therefore, year-to-year environmental variation and environmental heterogeneity may constrain evolution towards higher immune responsiveness.     

Manipulating rearing conditions reveals developmental sensitivity in the smaller sex of a passerine bird, the European starling Sturnus vulgaris

Traditionally, studies of sexually size-dimorphic birds and mammals report that the larger sex is more sensitive to adverse environmental conditions during ontogeny. However, recent studies in avian species that exhibit moderate size-dimorphism indicate that the smaller sex may be more sensitive to poor rearing conditions. To better understand sex-specific sensitivity in a passerine exhibiting moderate size-dimorphism, we examined growth, cell-mediated immunity (CMI) and survival of European starling Sturnus vulgaris nestlings following an experimental reduction of maternal rearing ability (via a feather-clipping manipulation). Contrary to conventional theory, daughters showed reduced growth in both body mass and measures of structural size in response to the maternal treatment. In contrast, sons showed no reductions in any of these traits in relation to the treatment. No sex-specific differences in nestling CMI were found for either group, although CMI of nestlings raised by manipulated mothers were higher than those of control nestlings. Finally, fledging sex ratios did not change from those at hatching indicating that neither sex appeared differentially sensitive to the maternal treatment in terms of mortality. These results reveal that variation in the quality of the rearing environment can have significant effects on the smaller sex of a passerine exhibiting moderate dimorphism and as such support recent studies of species with small-moderate sexual size-dimorphism. Combined results suggest that sex-specific effects of environmental variation on nestling development may be both context- (i.e., brood size, resource level, hatching order) and temporally- (when during development they occur) specific. Furthermore, more studies are needed that examine multiple traits at several developmental stages and then follow the sexes over the longer-term to examine potential effects on fitness.     

Avian cholera,post‐hatching survival and selection on hatch characteristics in a long‐lived bird,the common eider Somateria mollisima

Infectious diseases can have dramatic impacts on animal population dynamics, but how they influence vital rates remains understudied. We took advantage of the appearance of an avian cholera epizootic in an arctic colony of common eiders Somateria mollissima to study variation in juvenile survival and selection on hatch characteristics in relation to this highly infectious disease. Avian cholera is one of the most important infectious diseases affecting wild birds and is thought to primarily affect adult survival. Here, we show that avian cholera was associated with a 90% decline in duckling survival, leading to almost zero recruitment. Before the cholera outbreak, there was significant stabilizing selection on hatching date and significant positive directional selection on hatching mass. During cholera outbreaks, selection on hatch characteristics was no longer significant. These results were based on a low sample of surviving ducklings in cholera years, but suggested that date and mass at hatching did no longer affect duckling survival in the presence of cholera. These effects of avian cholera on post‐hatching survival were likely not only the consequence of the disease per se, but also a consequence of an increase in predation rates that followed the emergence of avian cholera. Our results emphasize the dramatic direct and indirect impacts that infectious disease can have on vital rates, and thus population dynamics.     

Laying order, hatching asynchrony and nestling body mass in Tree Swallows Tachycineta bicolor

We studied the reproductive biology of a box-nesting population of Tree Swallows Tachycineta bicolor in southeastern Wisconsin, USA. We were interested particularly in the relationship between laying order and hatching order and the extent to which each was a predictor of nestling body mass. We found that laying order was a significant predictor of hatching order. Laying and hatching order were related to nestling mass at 4 days of age and to a lesser extent at 12 days of age. In addition, we investigated the effects of natural variation in hatching asynchrony. Hatching asynchrony was positively related to the range of nestling body masses within a brood at days 4 and 12. The probability that brood reduction occurred was also positively related to the degree of hatching asynchrony, though this effect was significant only at day 4. Our results suggest that laying order and hatching order have their greatest effects on nestling Tree Swallows early in the nestling period.     

Eggshell pigmentation has no evident effects on offspring viability in common kestrels

Infectious diseases and parasitism are major environmental forces decreasing fitness, and thus individual strategies aimed at preventing pathogen infections, either in an individual or their offspring, should be favoured by natural selection. The mineral fraction and some organic compounds in the shells of bird eggs are considered physical and chemical barriers against pathogen penetration to the embryo. However, eggshell pigment deposition has only recently been considered as a mechanism to resist pathogen penetration into the egg. By wiping the eggshell surface, the amount of pigment and some cuticle proteins were experimentally manipulated for the first time in nature. The effects on egg hatchability and offspring viability measured as nestling condition, immunocompetence and probability of recruitment were investigated in the common kestrel Falco tinnunculus. Protoporphyrin IX and biliverdin IXα to a lesser extent were the only identified pigments. The concentration of protoporphyrin IX and cuticle proteins were significantly reduced in the wiped with respect to the control treatment. Our study shows no evidence of a detrimental effect of the reduction of eggshell pigments on egg hatchability, mortality of the chicks during the nesting period, nestling body condition, nestling local immune response to PHA antigen or probability of recruitment. Further research will be necessary to elucidate the direct role of protoporphyrins and other pigments in egg bacterial infection.     

Factors Affecting Growth of Tengmalm’s Owl (Aegolius funereus) Nestlings: Prey Abundance,Sex and Hatching Order

In altricial birds, energy supply during growth is a major predictor of the physical condition and survival prospects of fledglings. A number of experimental studies have shown that nestling body mass and wing length can vary with particular extrinsic factors, but between-year observational data on this topic are scarce. Based on a seven-year observational study in a central European Tengmalm’s owl population we examine the effect of year, brood size, hatching order, and sex on nestling body mass and wing length, as well as the effect of prey abundance on parameters of growth curve. We found that nestling body mass varied among years, and parameters of growth curve, i.e. growth rate and inflection point in particular, increased with increasing abundance of the owl’s main prey (Apodemus mice, Microtus voles), and pooled prey abundance (Apodemus mice, Microtus voles, and Sorex shrews). Furthermore, nestling body mass varied with hatching order and between sexes being larger for females and for the first-hatched brood mates. Brood size had no effect on nestling body mass. Simultaneously, we found no effect of year, brood size, hatching order, or sex on the wing length of nestlings. Our findings suggest that in this temperate owl population, nestling body mass is more sensitive to prey abundance than is wing length. The latter is probably more limited by the physiology of the species.     

The influence of sex and body size on nestling survival and recruitment in the house sparrow

Differences in the survival rates of males and females over the period from hatching to recruitment can have important impacts on individual fitness and population demographics. However, whilst the influence of an individual's sex on nestling growth and survival has been well studied, less is known about sex‐specific survival over the period between fledging and recruitment. Here, we analyse nestling survival and recruitment in an isolated, island population of house sparrows (Passer domesticus), using data collected over a 4‐year period. Nestlings that had a greater mass at 1 day old were more likely to fledge. Recruitment was also positively associated with day 11 mass. The positive influence of nestling mass on survival to fledging also increased as brood size increased. There was no difference in the survival of male and female individuals prior to fledging. In contrast, over the period from fledging to recruitment, females had significantly less mortality than males. Recruitment was also positively associated with 11‐day‐old mass. Neither the nestling sex ratio nor the fledging sex ratio deviated from 0.5, but the sex ratio amongst recruits was female biased. Our study shows that sex can influence juvenile survival, but also shows that its effect varies between different life‐history stages; therefore, these stages should be considered separately if we want to understand at what point sex‐specific differences in juvenile survival occur. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 680–688.     

Effects of intraclutch variation in egg size and hatching asynchrony on nestling development and survival in semi‐precocial Herring Gulls

Intraclutch egg size variation may non‐adaptively result from nutritional/energetic constraints acting on laying females or may reflect adaptive differential investment in offspring in relation to laying/hatching order. This variation may contribute to size hierarchies among siblings already established due to hatching asynchrony, and resultant competitive asymmetries often lead to starvation of the weakest nestling within a brood. The costs in terms of chick mortality can be high. However, the extent to which this mortality is egg size‐mediated remains unclear, especially in relation to hatching asynchrony which may operate concomitantly. I assessed effects of egg size and hatching asynchrony on nestling development and survival of Herring Gulls (Larus argentatus), where the smaller size and later hatching of c‐eggs may represent a brood‐reduction strategy. To analyze variation in egg size, I recorded the laying order and laying date of 870 eggs in 290 three‐egg clutches over a 3‐yr period (2010–2012). I measured hatchlings and monitored growth and survival of 130 chicks from enclosed nests in 2011 and 2012. The negative effect of laying date (β = ?0.18 ± SE 0.06, P = 0.002) on c‐egg size possibly reflected the fact that late breeders were either low quality or inexperienced females. The mass, size, and condition of hatchling Herring Gulls were positively related to egg size (all P < 0.0001). C‐chicks suffered from increased mortality risk during the first 12 d, identified as the brood‐reduction period in my study population. Although intraclutch variation in egg size was not directly related to patterns of chick mortality, I found that smaller relative egg size interactively increased differences in relative body condition of nestlings, primarily brought about by the degree of hatching asynchrony during this brood‐reduction period. Thus, the value of relatively small c‐eggs in Herring Gulls may lie in reinforcing brood reduction through effects on nestling body condition. A reproductive strategy Herring Gulls might have adopted to maintain a three‐egg clutch, but that also enables them to adjust the number of chicks they rear relative to the prevailing environmental conditions and to their own condition during the nestling stage.     

Seasonal decline in provisioning effort and nestling mass of Blue Tits Cyanistes caeruleus: experimental support for the parent quality hypothesis

A common feature of many birds breeding in seasonal environments is that fitness‐related parameters such as nestling mass or survival decline as the breeding season progresses. Consequently, there is a tendency for early breeders to have better reproductive performance than individuals breeding later in the season. This variation could be caused by factors associated with the date of laying, such as changing environmental conditions (date hypothesis), or by differences in parental quality between early and late breeders (parent quality hypothesis). To evaluate the relative importance of both hypotheses, we manipulated hatch dates of Blue Tits Cyanistes caeruleus by exchanging clutches with different incubation stages and assessed the impact on nestling mass, nestling diet and provisioning rates. Mean nestling mass declined significantly over the season. This was the combined result of differences in parental quality, which dominated in the early part of the season, and the influence of hatching date (date effect per se), which prevailed later in the season. Nestling diet composition was apparently uninfluenced by the manipulation, suggesting that deteriorating food supplies are the primary reason for the seasonal variation in the nestling diet. Counter to the date hypothesis, delayed parents did not feed their young less than control pairs did, but in fact exhibited higher provisioning rates. Our results suggest that in this population, parental quality seems to constrain post‐hatching reproductive performance and such intrinsic limitations may help to explain why certain individuals breed later.     

Reduced compensatory growth capacity in mistimed broods of a migratory passerine

Phenotypic plasticity has recently been proposed to increase population viability when rapid anthropogenic environmental changes cannot be tracked by means of evolution. This assumes that environmental changes do not constrain phenotypic plasticity itself, which has rarely been examined in natural populations. In areas of climate warming, many long-distance migratory birds breed increasingly late relative to the period of peak food supply, and the temporal mismatch may constrain plastic life-history traits such as nestling growth. We combined 23 years of food availability and breeding data with a 3-year experimental manipulation of nestling growth trajectories in a Central European population of collared flycatchers (Ficedula albicollis) to examine the potential impact of climate-related mistimed breeding on nestling developmental plasticity. Timing of the food peak was predicted by winter climate, and the median hatching date of broods was earlier in springs with earlier food peaks. However, the adjustment of hatching date was incomplete and the population largely missed the food peak in years with very early food peaks. After imposing a temporary, experimental food shortage on nestlings, the extent of compensatory growth in body mass differed among years, and this difference was apparently related to the distance of hatching dates from the yearly food peak. Growth compensation declined with distance from the peak. These results suggest that mistimed phenology may not only create permanently adverse conditions for migratory species but it may also constrain the plastic responses of individuals to temporary disturbances. Therefore, climate change may not only favour but also restrict phenotypic plasticity.     

Mhc polymorphisms fail to explain the heritability of phytohaemagglutinin-induced skin swelling in a wild passerine

Genetic estimates of the variability of immune responses are rarely examined in natural populations because of confounding environmental effects. As a result, and because of the difficulty of pinpointing the genetic determinants of immunity, no study has to our knowledge examined the contribution of specific genes to the heritability of an immune response in wild populations. We cross-fostered nestling house sparrows to disrupt the association between genetic and environmental effects and determine the heritability of the response to a classic immunological test, the phytohaemagglutinin (PHA)-induced skin swelling. We detected significant heritability estimates of the response to PHA, of body mass and tarsus length when nestlings were 5 and 10 days old. Variation at Mhc genes, however, did not explain a significant portion of the genetic variation of nestling swelling to PHA. Our results suggest that while PHA-induced swelling is influenced by the nest of origin, the importance of additive genetic variation relative to non-additive genetic variation and the genetic factors that influence the former in wild populations still need to be identified for this trait.