Parental and genetic factors rather than nesting forest patch size affect physiological traits of offspring in an area‐sensitive passerine: an experimental study

Our understanding of the effects of habitat loss on individual performance is limited due to a lack of experimental studies that take the potential genetic and parental effects producing phenotypic variation into consideration. To assess the relative role of habitat loss on offspring phenotype while controlling for the confounding effects of genetic and parental variation we performed a partial cross‐fostering experiment using the Eurasian Treecreeper Certhia familiaris. The experiment was carried out by swapping half the nestlings in a brood between small and large nesting forest patches to determine the effect of nesting forest patch size on five nestling traits reflecting morphological size, body condition, physiological stress and inflammation status. There was no effect of nesting forest patch size on the offspring traits examined. Instead, we found evidence of genetic and early parental effects on all traits except inflammation status, as well as parental effects after cross‐fostering for all of the measured offspring traits. Our results suggest that genetic and parental effects should be taken into account when making inferences about species’ responses to habitat loss.     

Causes and consequences of adaptive seasonal sex ratio variation in house sparrows

1. Here we examine how sex ratio variation in house sparrow broods interacts with other demographic traits and parental characteristics to improve the understanding of adaptive significance and demographic effects on variation in sex ratio. 2. The sex ratio in complete broods did not deviate significantly from parity (54.9% males). 3. There was sex-specific seasonal variation in the probability of recruitment. Male nestlings that hatched late in the breeding season had larger probability of surviving than early hatched males. 4. An adaptive adjustment of sex ratio should favour production of an excess of males late in the breeding season. Accordingly, the proportion of male offspring increased throughout the breeding season. 5. A significant nonlinear relationship was present between sex ratio and age of the female. However, there was no relationship between parental phenotype and standardized hatch day that could explain the observed seasonal change in sex ratio. 6. The sex-specific number of offspring recruited by a pair to subsequent generations was closely related to the brood sex ratio. 7. These results indicate an adaptive adjustment of sex ratio to seasonal variation in environmental conditions that affects the offspring fitness of the two sexes differently. Our results also suggest that such a sex ratio variation can strongly influence the demography and structural composition of small passerine populations.     

Epigenetics and parental effects

Parental effects are a major source of phenotypic plasticity and may influence offspring phenotype in concert with environmental demands. Studies of “environmental epigenetics” suggest that (1) DNA methylation states are variable and that both demethylation and remethylation occur in post‐mitotic cells, and (2) that remodeling of DNA methylation can occur in response to environmentally driven intracellular signaling pathways. Studies of mother‐offspring interactions in rodents suggest that parental signals influence the DNA methylation, leading to stable changes in gene expression. If parental effects do indeed enhance the “match” between prevailing environmental demands and offspring phenotype, then the potential for variation in environmental conditions over time would suggest a mechanism that requires active maintenance across generations through parental signaling. We suggest that parental regulation of DNA methylation states is thus an ideal candidate mechanism for parental effects on phenotypic variation.     

Effect of altitude on male parental expenditure in Mountain Bluebirds ( Sialia currucoides ): are higher-altitude males more attentive fathers?

Male investment of time and energy in caring for offspring varies substantially both between and within bird species. Explaining this variation is of long-standing interest to ornithologists. One factor that may affect male care is breeding site altitude, through its effects on climate. The harsher, less predictable abiotic conditions at higher altitudes are hypothesized to favour increased male investment of time and energy in offspring care. We tested this hypothesis by comparing male parental behaviour in Mountain Bluebirds (Sialia currucoides) nesting at 1500 and 2500 m a.s.l. in the Bighorn Mountains of Wyoming, USA. We compared rates of prey delivery to nestlings at these two altitudes at two times: 1–2 days after hatching, when females spend much of their time brooding young, and 12–13 days later, when brooding has ended and nestling energy demands are peaking. High-altitude males fed nestlings 18 and 28% more often than low-altitude males early and later in the nestling stage, respectively, but only the difference in late-stage feeding rates were significant. Like males, females at the high site also fed nestlings significantly more often than females at the low site later in the nestling stage (45% difference in feeding rates). Consequently, the proportion of all feeding trips made by males at the high site (40%) did not differ significantly from that at the low site (44%). Parents at the high altitude may feed nestlings more often to compensate for their greater thermoregulatory costs. Parents may also be attempting to assist nestlings in storing fat and/or attaining a large size and effective homeothermy as quickly as possible to enhance nestling ability to survive bouts of severe weather which are common at high altitudes.     

Coadaptation of offspring begging and parental provisioning: A role for prenatal maternal effects?

Recent studies on birds have shown that offspring begging and parental provisioning covary at the phenotypic level, which is thought to reflect genetic correlations. However, prenatal maternal factors, like yolk testosterone, may also facilitate parent-offspring coadaptation via their effects on offspring begging and development. In fact, maternal effects are thought to adjust offspring phenotype to the environmental conditions they will experience after birth, which are in turn strongly dependent on the levels of parental provisioning. Using cross-fostering experiments in canaries, we tested the role of maternal effects on parent-offspring coadaptation from two different approaches. First, we analyzed whether females deposit yolk testosterone in relation to their own or their partner's prospective parental provisioning, measured as the rate of parental feeding to foster nestlings. Second, we investigated whether females deposit yolk testosterone in relation to costs they incurred when raising a previous brood, as this likely impinges on their capacity to provide parental care in the near future. However, from the results of both experiments we have no evidence that canary females deposit yolk testosterone in order to match offspring begging to the levels of care they and/or their partners provide. We therefore found no evidence that yolk testosterone facilitates parent-offspring coadaptation. In addition, our results suggest that the functional consequences of yolk testosterone deposition may relate to hatching asynchrony since it primarily varied with egg laying order.     

Costs and Benefits of Competitive Traits in Females: Aggression,Maternal Care and Reproductive Success

Recent research has shown that female expression of competitive traits can be advantageous, providing greater access to limited reproductive resources. In males increased competitive trait expression often comes at a cost, e.g. trading off with parental effort. However, it is currently unclear whether, and to what extent, females also face such tradeoffs, whether the costs associated with that tradeoff overwhelm the potential benefits of resource acquisition, and how environmental factors might alter those relationships. To address this gap, we examine the relationships between aggression, maternal effort, offspring quality and reproductive success in a common songbird, the dark-eyed junco (Junco hyemalis), over two breeding seasons. We found that compared to less aggressive females, more aggressive females spent less time brooding nestlings, but fed nestlings more frequently. In the year with better breeding conditions, more aggressive females produced smaller eggs and lighter hatchlings, but in the year with poorer breeding conditions they produced larger eggs and achieved greater nest success. There was no relationship between aggression and nestling mass after hatch day in either year. These findings suggest that though females appear to tradeoff competitive ability with some forms of maternal care, the costs may be less than previously thought. Further, the observed year effects suggest that costs and benefits vary according to environmental variables, which may help to account for variation in the level of trait expression.     

Body condition variation in kestrel (<Emphasis Type="Italic">Falco tinnunculus</Emphasis>) nestlings in relation to breeding conditions

The body condition index (i.e., body mass corrected for age or size differences) is commonly used to investigate offspring condition in nestling birds. The body condition index reflects different parameters related to the general nutritional state of nestlings and may predict survival prospects. Since conditions experienced during the growth period can affect the fitness of nestlings in adulthood, we investigated proximate and ultimate factors underlying body condition index variation in kestrel (Falco tinnunculus) nestlings in a 9-year field study and we carried out two cross-fostering experiments to disentangle the origin (genetics plus maternal effects) and rearing (environment effect) components of body condition index variation. In total, we sampled 2,065 nestlings from 464 broods and used 121 nestlings from 24 broods in the cross-fostering experiments. We found that nestlings from larger broods had higher body condition index than nestlings from smaller ones, but this pattern did not emerge in two of the 9 years of study; nestlings born later in the breeding season had lower body condition index in some years but not in others; the decrease of body condition index over the breeding season emerged in all but three-chick broods; males and females did not differ neither in body condition index nor in the covariation between body mass and wing length, while this result was limited to one of the nine field study years; the annual mean value of body condition index did not covary with the total rainfall; both the origin and rearing components explained body condition index variation, but their relative contributions varied from a year to another. Overall, these results suggest that the brood size is not a good predictor of body condition index; the rule “nesting early in the season is better” is less general than previously thought; the body condition index may contain origin variance, whose expression may be modulated by environmental conditions.     

Individual variation in parental tradeoffs between the number and size of offspring at the pre- and post-natal stages

Life-history theory predicts that parents refer to the resources they hold to determine their breeding strategy. In multi-brooded species, it is hypothesized that single-brooded parents produce larger clutches and raise offspring with a brood survival strategy, whereas multi-brooded parents only do this under good breeding conditions. Under poor conditions, they produce smaller clutches and raise offspring with a brood reduction strategy. We tested this hypothesis in the Brown-cheeked Laughing Thrush Trochalopteron henrici, which can breed twice a year on the Tibetan Plateau, by investigating the life-history traits and provisioning behaviours of single- and double-brooded parents. Single-brooded parents laid larger clutches of smaller eggs and produced more and larger fledglings than double-brooded parents in their first brood. Double-brooded parents produced smaller clutches of larger eggs but fledged larger nestlings in their first brood than in their second brood. As single-brooded parents only need to raise one brood a year, then producing and raising as many offspring as possible (i.e. the brood survival strategy in a large brood) can maximize their reproductive success. For double-brooded parents, producing and raising fewer offspring in the first brood (i.e. the brood survival strategy in a small brood) can ensure their nesting success during a short breeding cycle. Additionally, producing more offspring but raising larger nestlings in the second brood (i.e. the brood reduction strategy in a large brood) can select for offspring of higher quality within the brood. Our findings indicate that different tradeoffs between single- and double-brooded parents in egg-laying and nestling-raising may be an adaptation to the seasonal variation in environmental conditions.     

Environmental effects on variation and covariation in reproductive traits of Western Bluebirds

Summary Environmental conditions can influence the expression and correlations of phenotypic traits. I studied phenotypic plasticity in reproductive traits of Western Bluebirds breeding in northern Arizona. Data collected over 4 years on two contrasting habitats identified significant spatial and temporal variation in bluebird reproduction. Clutch size was similar over different environmental conditions whereas timing of clutch initiation, percent fledging success, and frequency of second nest attempts were flexible. Correlations between traits varied widely—often changing sign—among samples from different years or habitats. Correlations of traits with reproductive success were also dependent on environmental conditions. Variation in traits reflected behavioral responses by nesting adults to differences in time for breeding and feeding conditions. Density of trees differed between habitats and had opposing effects on these environmental variables; breeding seasons were generally longer, but feeding rates to nestlings were lower on the more open habitat. Late Spring snows delayed reproduction and increased the importance of limited time for breeding; feeding conditions were more influential following a dry Spring. This and other studies illustrate that data on phenotypic plasticity are important when evaluating the ecological and evolutionary forces underlying life histories.     

Alarm calls of the Southern House Wren Troglodytes musculus: variation with nesting stage and predator model

Alarm calls given by parents when risk is detected during nesting may be considered a form of parental defense. We analyzed variations in callings of breeding pairs of the Southern House Wren Troglodytes musculus during the nesting cycle and when faced with different predator models. Nesting birds were exposed to stuffed models at different nesting stages (early and late during incubation, and nests with younger and older nestlings). Nests were also exposed to different predator models where the calling response of breeding adults and acoustic structure variations of the calls were analyzed. The presence of a predator model increased the parents’ alarm calls along the nesting stage. This result supports the hypothesis that the higher the nest reproductive value, the higher the nest defense performed by the Southern House Wren. However, it also supports the notion that alarm calls could be used by parents to silence nestlings and reduce their detectability. Alarm calls also varied according to the predator model presented. We suggest that alarm calls variations of Southern House Wrens could encode information about the kind of predator and the risk envisaged through variations of call rates.     

Anthropogenically-Mediated Density Dependence in a Declining Farmland Bird

Land management intrinsically influences the distribution of animals and can consequently alter the potential for density-dependent processes to act within populations. For declining species, high densities of breeding territories are typically considered to represent productive populations. However, as density-dependent effects of food limitation or predator pressure may occur (especially when species are dependent upon separate nesting and foraging habitats), high territory density may limit per-capita productivity. Here, we use a declining but widespread European farmland bird, the yellowhammer Emberiza citrinella L., as a model system to test whether higher territory densities result in lower fledging success, parental provisioning rates or nestling growth rates compared to lower densities. Organic landscapes held higher territory densities, but nests on organic farms fledged fewer nestlings, translating to a 5 times higher rate of population shrinkage on organic farms compared to conventional. In addition, when parental provisioning behaviour was not restricted by predation risk (i.e., at times of low corvid activity), nestling provisioning rates were higher at lower territory densities, resulting in a much greater increase in nestling mass in low density areas, suggesting that food limitation occurred at high densities. These findings in turn suggest an ecological trap, whereby preferred nesting habitat does not provide sufficient food for rearing nestlings at high population density, creating a population sink. Habitat management for farmland birds should focus not simply on creating a high nesting density, but also on ensuring heterogeneous habitats to provide food resources in close proximity to nesting birds, even if this occurs through potentially restricting overall nest density but increasing population-level breeding success.     

Seasonal variation in food availability influences the breeding strategy of White‐collared Blackbirds Turdus albocinctus on the Tibetan Plateau

Parent birds show a continuous spectrum of breeding strategies, ranging from a low‐fecundity and high‐survival pattern to a high‐fecundity, low‐survival pattern. Investigations of parental breeding strategies under variable environmental conditions can illustrate how parents trade‐off the benefits and costs of these two extreme strategies. White‐collared Blackbirds Turdus albocinctus can breed twice a year on the Tibetan Plateau. We show that both life‐history traits and parental feeding behaviour differ between these two breeding attempts. In the first attempt, the birds produced small clutches and fledged a small number of nestlings of high body condition. In the second attempt, they produced larger clutches and fledged more nestlings of lower body condition. Males made greater contributions to brood provisioning compared with females in the first attempt but there was no sex difference in brood provisioning in the second attempt. In the first attempt, producing smaller clutches can shorten the nestling period, and the increased male contribution to brood provisioning can protect the energy reserves of females. Thus, females can begin a second attempt sooner and produce larger clutches. During the second nesting attempt, when conditions are warmer and wetter, parents rely on a broader array of food types (both invertebrates and plant material, primarily berries) than during the first attempt, which includes only animal food such as arthropods and annelids. We suggest that this difference in breeding strategies between nesting attempts and sexes is in part influenced by marked seasonal variation in food availability.     

Is the blue tit falling into an ecological trap in Argentine ant invaded forests?

Because insectivorous birds must evaluate resources for reproduction before settling into a breeding habitat, they can fall into an ecological trap if informative cues about habitat suitability become dissociated from their actual yield. Given their potential to affect ecological networks, invasive ant species are potential candidates for triggering such ecological traps. We combined observational and experimental approaches to examine whether the variation in food supply for nestlings resulting from the invasion of the Argentine ant, Linepithema humile, had any influence on the breeding ecology of the blue tit, Cyanistes caeruleus, an insectivorous foliage-gleaner. We investigated the effects of the ant invasion on breeding performance (nesting success, clutch size, brood size and breeding success) and offspring quality (body size and condition, developmental stability and plumage colour) in replicated Mediterranean forest areas over a period of 3 years. There was no evidence that the reduction in caterpillar availability resulting from the invasion had a concurrent negative effect on the blue tit’s ability to successfully rear nestlings in optimal conditions, at least as measured here. Although the raw figures suggest an increased level of nutritional stress in blue tits breeding in invaded forests, the data analyses showed no significant alterations in terms of productivity or offspring fitness. The reproductive performance of the blue tit has been shown to be remarkably resilient to the Argentine ant-mediated food shortage, either because the prey reduction following the invasion did not reach a critical threshold or because of compensatory activity by the progenitors. We cannot conclusively reject an ecological trap triggered by the ant invasion on blue tits, since neither fledgling recruitment nor the prospective survival of parents were assessed. Even though we could not confirm short-term consequences of the Argentine ant invasion on blue tit reproductive fitness, the long-term bottom-up effects of the invasion remain unknown and should not be ruled out.     

Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population

Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.     

Developmental stress increases reproductive success in male zebra finches

There is increasing evidence that exposure to stress during development can have sustained effects on animal phenotype and performance across life-history stages. For example, developmental stress has been shown to decrease the quality of sexually selected traits (e.g. bird song), and therefore is thought to decrease reproductive success. However, animals exposed to developmental stress may compensate for poor quality sexually selected traits by pursuing alternative reproductive tactics. Here, we examine the effects of developmental stress on adult male reproductive investment and success in the zebra finch (Taeniopygia guttata). We tested the hypothesis that males exposed to developmental stress sire fewer offspring through extra-pair copulations (EPCs), but invest more in parental care. To test this hypothesis, we fed nestlings corticosterone (CORT; the dominant avian stress hormone) during the nestling period and measured their adult reproductive success using common garden breeding experiments. We found that nestlings reared by CORT-fed fathers received more parental care compared with nestlings reared by control fathers. Consequently, males fed CORT during development reared nestlings in better condition compared with control males. Contrary to the prediction that developmental stress decreases male reproductive success, we found that CORT-fed males also sired more offspring and were less likely to rear non-genetic offspring compared with control males, and thus had greater overall reproductive success. These data are the first to demonstrate that developmental stress can have a positive effect on fitness via changes in reproductive success and provide support for an adaptive role of developmental stress in shaping animal phenotype.     

Nest predation and habitat change interact to influence Siberian jay numbers

We studied Siberian jays, breeding in northern Sweden, to examine the potential for interactions between nest predation and reduced vegetation heterogeneity around nest sites to cause a decrease in jay numbers. Parent behaviour and nests are highly cryptic in the species. Our 12-year data showed, however, that nests had a probability of only 0.46 to be successful and produce at least one nestling. Nest predation was intense and a main cause of nest failure. All predators that could be identified were visually oriented hunters, mostly other corvids able to colonize taiga forest only close to human settlements. Consistent with the idea that predators used visual cues, nest predation increased with parental activity, which suggests that predators used parental provisioning trips to locate nests. Furthermore, a reduction in daily nest survival rates with decreasing amount of nesting cover was more pronounced in areas with high corvid activity as predicted when cover mediates the hunting efficiency of visual oriented predators. Declining temperatures interacted with the effects of habitat characteristics to further reduce daily nest survival rates suggesting that parents were not able to increase nest visitation rates to satisfy the higher energy demands of their nestlings without endangering the nest. Our results identify a mechanism through which predation and human-induced reduction in nesting cover on a larger scale may interact to cause a reduction in Siberian jay numbers larger than expected from habitat loss alone.     

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care.

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.     

Implications of nest-site limitation on density-dependent nest predation at variable spatial scales in a cavity-nesting bird

Nest‐site limitation may have different implications in the spatial distribution of breeding pairs depending on the availability of suitable habitat and the types of nest‐sites. Distribution of cavities suitable as nest sites may allow circumstantial aggregation or active choice of colonial nesting, which may have different implications on breeding performance through effects on breeding density, with variable costs and benefits depending on the consequences of intraspecific competition, social interactions and predation. We evaluated the effects of breeding density derived from nesting site limitation on breeding performance and predation at different spatial scales and considering multiple social, population and environmental limiting factors in the red‐billed chough Pyrrhocorax pyrrhocorax. The results indicate that variable breeding density may arise within the population depending on the availability and spatial distribution of nest‐sites. Nest‐site availability and distribution may also determine social breeding systems (isolated or aggregated) at variable densities, thus resembling differences found at different spatially distant populations under contrasting environmental conditions. Breeding performance was related to density‐dependent processes of population regulation, especially density‐dependent nest predation due to predator attraction to nest clusters. Results also indicate that predation pressure depend on density patterns at large scales. This suggest that predation may have important consequences on population dynamics of spatially structured populations depending on the strength of this kind of density dependence, which in turn may depend on habitat features affecting the prey but also the spatially variable guild of predators. Because habitat and nesting site availability may vary spatially depending on multiple human influences, understanding the strength and form in which breeding density and nest predation at different spatial scales may influence the size and persistence of populations can help to manage them more adequately.     

Resource availability, breeding site selection, and reproductive success of red-winged blackbirds

Red-winged blackbirds are polygynous and show strong breeding site preferences, but it is unclear which environmental factors regulate their reproductive success and are ultimately responsible for shaping their patterns of habitat selection and their mating system. We evaluated the effect of variation in insect emergence rates on the reproductive success of male and female redwings nesting on replicate ponds. The number of male and female redwings that settled on a pond varied two- to three-fold among ponds, but was not related to insect emergence rates. Insect emergence rates had a positive effect on the number of nestlings successfully fledged by females, the number of nestlings fledged from male territories, and on the mass of nestlings at fledging. Typha stem density also varied widely among ponds, and was positively related to male and female settling density and mass of nestlings at fledging, but not to the number of nestlings fledged by females or males. We conclude that alternative breeding sites differ in their ability to support redwing reproduction, and that the availability of emerging odonates is an important environmental factor influencing the reproductive success of both male and female red-winged blackbirds. Received: 31 March 1997 / Accepted: 3 July 1997     

Long-term consequences of early ontogeny in free-living Great Tits Parus major

Environmental factors during early development may have profound effects on subsequent life-history traits in many bird species. In wild birds, sex-specific effects of early ontogeny on natal dispersal and future reproduction are not well understood. The objective of this work was to determine whether hatching date and pre-fledging mass and condition of free-living Great Tits Parus major have any subsequent effect on individuals’ natal dispersal and reproductive performance at first breeding. Both males and females dispersed longer distances in coniferous than in deciduous forests, while dispersal was condition-dependent only in males (heavier as nestlings dispersed farther). In females, mass and condition at pre-fledging stage correlated significantly with clutch size, but not with subsequent reproductive performance as measured by fledging success or offspring quality. In contrast, heavier males as nestlings had higher future fledging success and heavier offspring in their broods compared with those in worse condition as nestlings. The hatching date of female as well as male parents was the only parental parameter related to the number of eggs hatched at first breeding. These results indicate that pre-fledging mass and condition predict subsequent fitness components in this bird species. We suggest that sex-specific relationships between a disperser’s condition and its selectivity with respect to breeding habitat and subsequent performance need to be considered in future models of life-history evolution.