Calcium effects on life-history traits in a wild population of the great tit (Parus major): analysis of long-term data at several spatial scales

Calcium is an essential micronutrient for birds during egg formation and for skeletal development in nestlings. Habitat level studies suggest that birds breeding in low-calcium areas may be limited in the size or number of eggs they lay and in the quality of their nestlings. However, as birds forage non-randomly and may travel considerable distances to acquire calcium, describing different breeding environments in terms of their calcium availability is problematic. Here we explore the spatial relationships between 300-fold variation in soil calcium and the life-history traits of ca. 6,000 pairs of great tits breeding in a single continuous woodland over 41 years. Controlling for other habitat differences, we found strong positive associations between soil calcium, clutch size and recruitment at spatial scales of over 300 m from each nestbox, suggesting that females may have been travelling inter-territorially to acquire calcium during egg formation. Soil calcium near each nestbox (mean distance = 58 m) was a strong positive predictor of mean fledgling mass, suggesting that local calcium was more important during nestling stages. We found no effect of soil calcium on lay-date or egg mass. This study is the first to provide evidence that small woodland passerines are limited by calcium availability at several different spatial scales. However, experimental work is necessary to test the causality of these spatial patterns.     

Components of variance underlying fitness in a natural population of the great tit Parus major

Traits that are closely associated with fitness tend to have lower heritabilities (h2) than those that are not. This has been interpreted as evidence that natural selection tends to deplete genetic variation more rapidly for traits more closely associated with fitness (a corollary of Fisher's fundamental theorem), but Price and Schluter (1991) suggested the pattern might be due to higher residual variance in traits more closely related to fitness. The relationship between 10 different traits for females, seven traits for males, and overall fitness (lifetime recruitment) was quantified for great tits (Parus major) studied in their natural environment of Wytham Wood, England, using data collected over 39 years. Heritabilities and the coefficients of additive genetic and residual variance (CVA and CVR, respectively) were estimated using an "animal model." For both males and females, a trait's correlation (r) with fitness was negatively related to its h2 but positively related to its CVR. The CVA was not related to the trait's correlation with fitness in either sex. This is the third study using directly measured fitness in a wild population to show the important role of residual variation in determining the pattern of lower heritabilities for traits more closely related to fitness.     

Genetic variability in mitochondrial DNA in a regional population of the great tit (Parus major)

Genetic variation of mitochondrial DNA (mtDNA) in 18 great tits (Parus major) from three neighboring localities in Sweden was investigated with eight tetranucleotide restriction endonucleases. The 18 individuals could be separated into 13 different maternal lineages. The high number of female lineages present in this regional population contrasts with a low level of sequence divergence between the different mtDNA clones, with a mean of 0.19% sequence divergence between all individuals. There was no obvious spatial structuring of mtDNA clones among the three localities. The presence of a high number of different clones with a low degree of sequence divergence could be explained by the effects of a large long-term effective population size, with the mtDNA clones having diverged about 25,000–200,000 years ago.This study was supported by the Swedish Natural Science Research Council, the Erik Philip-Sörensen Foundation, and the Nilsson-Ehle Foundation.     

Density effects on life-history traits of an island lizard population

Long-term monitoring of life-history traits and the effects of density upon them were studied in an island population of the lizardEumeces okadae. Although life-history traits such as clutch size, egg size and the proportion of mature reproductive females varied little over 7 years in the intact population, manipulation of density to simulate decreased population density enhanced juvenile growth rate, age at first reproduction, frequency of female reproduction and size-specific clutch mass. In particular, the proportion of mature females reproducing annually increased almost 10 times from 5.6% to 53.8% after the removal of some lizards. However, body size at first reproduction and egg size were almost identical under both high and low density conditions. This study suggests that there were strong density-dependent effects on several life-history traits and thatE. okadae attained a density close to the carrying capacity of the environment.     

Speckled eggs: water-loss and incubation behaviour in the great tit Parus major

Many small passerine birds worldwide lay white eggs speckled with red, brown and black protoporphyrin pigment spots (maculation). Unlike some patterns of avian eggshell pigmentation which clearly serve a crypsis or signalling function, the ubiquity of maculation among passerines suggests that its origins lie in another function, not specific to any particular ecological or behavioural group. Elsewhere, we have presented evidence that protoporphyrin pigments serve a structural function related to eggshell thickness and calcium availability: eggshell maculation in the great tit Parus major increases with decreasing soil calcium levels, pigments demarcate thinner areas of shell, and both the pigment intensity and distribution are related to shell thickness. Here we show that maculation also affects the rate of water loss from the egg during incubation (≈ Mass Loss per Day or MLD, which is critical to egg viability), but not that of unincubated eggs. We also demonstrate, both by observation and experiment, that the effect of female incubation behaviour on MLD compensates in some way for variation in egg characteristics, and that differences between females in the degree of such compensation are related to differences in clutch maculation. Our results suggest that, while a principal function of maculation in this species may be to strengthen the eggshell, it may also reduce eggshell permeability when large amounts of pigment are used, and that this necessitates a behavioural adjustment from the female during incubation. We discuss these findings and make further testable predictions from our model.     

Paternal leakage of mitochondrial DNA in the great tit (Parus major)

Animal mitochondrial DNA is normally inherited clonally from a mother to all her offspring. Mitochondrial heteroplasmy, the occurrence of more than one mitochondrial haplotype within an individual, can be generated by relatively common somatic mutations within an individual, by heteroplasmy of the oocytes, or by paternal leakage of mitochondria during fertilization of an egg. This biparental inheritance has so far been reported only in mice, mussels, Drosophila, and humans. Here we present evidence that paternal leakage occurs in a bird, the great tit Parus major. The major and minor subspecies groups of the great tit mix in the middle Amur Valley in far-eastern Siberia, where we found a bird that possessed the very distinct haplotypes of the two groups. To our knowledge this is the first report of paternal leakage in birds.     

Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population

Studies of a range of taxa, including birds, have revealed latitudinal clines in allele length at the conserved Clock locus, a gene with known influences on behaviour and physiology. Such clines might reflect adaptation to seasonal variation, a suggestion supported by a recent within‐population analysis of blue tits Cyanistes caeruleus, which found associations between Clock genotype and timing of breeding in females. To test the generality of this pattern, we sequenced the polymorphic poly‐Q locus of the Clock gene in 521 female great tits Parus major, which were selected based on possession of extreme breeding phenotypes. In total, we identified five alleles with one allele accounting for 96% of allelic diversity in the sample set. Overall variability at the poly‐Q locus was very low, and the spatial distribution of Clock alleles across Wytham was highly homogenous. Our data further provide no evidence for a connection between Clock genotype and reproductive timing phenotype in female great tits; further, we found no effect of Clock genotype on reproductive success. Hence, these results are in contrast to the pattern found for the sympatric blue tit population inhabiting the same woodlands, suggesting that phenotypic effects of Clock are not general in passerine birds.     

Offspring sex ratio is related to male body size in the great tit (Parus major)

Sex allocation theory predicts that the allocation of resourcesto male and female function should depend on potential fitnessgain realized through investment in either sex. In the greattit (Parus major), a monogamous passerine bird, male resourceholdingpotential (RHP) and fertilization success both depend on malebody size (e.g., tarsus length) and plumage traits (e.g., breaststripe size). It is predicted that the proportion of sons ina brood should increase both with male body size and plumage traits,assuming that these traits show a father—offspring correlation. Thiswas confirmed in our study: the proportion of sons in the brood increasedsignificantly with male tarsus length and also, though not significantly,with the size of the breast stripe. A sex ratio bias in relationto male tarsus length was already present in the eggs because(1) the bias was similar among broods with and without mortalitybefore the nestlings' sex was determined, and (2) the bias remainedsignificant when the proportion of sons in the clutch was conservativelyestimated, assuming that differential mortality before sex determinationcaused the bias. The bias was still present among recruits.The assumption of a father—offspring correlation was confirmedfor tarsus length. Given that both RHP and fertilization successof male great tits depend on body size, and size of father andoffspring is correlated, the sex ratio bias may be adaptive.     

Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major

Inbreeding depression has been hypothesized to drive the evolutionof mating systems and dispersal. Some studies have shown thatinbreeding strongly affects survival and/or fecundity, but otherstudies suggest that fitness consequences of inbreeding areless detrimental or more complex. We studied consequences ofmating with a relative in a population of great tits (Parusmajor) with a high local recruitment rate. Genotypic informationfrom microsatellite markers was used to calculate coefficientsof kinship, and fitness was measured as seasonal and lifetimereproductive success. We show that mating with a relative affectsseasonal reproductive success, as was found in other studiesof the same species. However, these effects do not result ina lifetime fitness reduction, suggesting that individuals mayhave scope for avoidance of inbreeding after inbreeding depression.Several explanations are proposed as compensatory mechanisms.Although individuals are more likely to divorce after experiencinginbreeding depression, we show that divorce alone cannot explainthe compensation for inbreeding depression in subsequent breedingattempts in our study. We conclude that the costs of matingwith a relative in the short term do not necessarily imply lifetimefitness consequences.     

Caterpillar abundance in the territory affects the breeding performance of great tit Parus major minor

The effects of caterpillar food supply on the breeding performance of a population of the Japanese great tit Parus major minor were investigated. Since more than 90% of the food items in our study site were caterpillars living on trees, we estimated the food availability using 20 frass traps per hectare. The sampling error of this method was about 10% on average, which was accurate enough to detect differences between territories. Food abundance at laying in each territory affected the timing of egg laying. However, food amount after hatching was correlated with clutch size. No relationship was found between fledgling quality and food availability, probably because the effects of local variation in food abundance could be canceled out by parental effort such as extending the foraging area. There was a significant negative correlation between the length of the nestling period and food availability. We suggest that parent tits decide the timing of fledging at the point where two factors, predation risk before fledging and additional improvement of nestling quality, are balanced. Food availability just after fledging affected the length of post-fledging parental care; it seems that fledglings in “poor” territories would have had difficulty in finding food and hence needed to depend on their parents longer than those in “rich” territories. Received: 10 June 1997 / Accepted: 29 December 1997     

Effects of snow cover on the social and foraging behavior of the great tit Parus major

In the Joetsu region of central Honshu, Japan, snow lies on the ground 2–3 m deep from January to February every year. To test the effects of snow cover on the social and foraging behaviors of the great tit (Parus major Linnaeus) in the region, the following parameters were compared between the pre-snowy period (November and December) and the snowy period (January and February) at the individual level: population size, monospecific flock size and the stability of its membership, home range size, attendance rate with mixed-species flocks, and foraging height. Great tits lived alone or in pairs, but often joined mixed-species flocks. Throughout the study period, individuals exhibited strong site fidelity, which resulted in a stable population size. Neither the size of a monospecific flock nor its membership was affected by snow cover. The home range expanded when birds joined mixed-species flocks during both periods. Birds more frequently joined mixed-species flocks during the snowy period, and the size of mixed-species flocks was significantly larger than during the pre-snowy period. During the snowy period, birds shifted their foraging position from the ground to the upper parts of trees. They also used the upper parts of trees when they joined mixed-species flocks. These results suggest that the intraspecific sociality of great tits is relatively insensitive to snow cover, but that the home range size and foraging positions are affected by joining mixed-species flocks, rather than by snow cover.     

Brood defense and brood size in the great tit (Parus major): a test of a model of unshared parental investment

To understand the interaction of the many contextual variablesthat affect parental behavior a number of static optimalitymodels have been developed. Among these the one by Lazarus andInglis (1986) is the only one to specifically predict the magnitudeof unshared parental investment (PI), i.e., of parental carethat carries a cost to the parent and that benefits all currentoffspring equally because it cannot be divided among them. Weinvestigated specifically how parent great tits (Parus major)gear their brood defense, a form of unshared PI, to the sizeof the brood at stake and to the risk incurred as a functionof the type of predator. The predators used were dummies ofthe great spotted woodpecker (Picoides major) and of the tawnyowl (Strix aluco). Normally, adults can approach the woodpeckerwith impunity; it had inflicted heavy losses to nestlings ofthe study populations of great tits near Wolfsburg, Lower Saxony.Parent great tits whose brood had been artificially reducedto two young responded to the dummy with less defense than dida control group with their pre-test brood size left intact.The nature of defense was qualitatively the same as that elicitedby a live woodpecker. Parents confronting the owl near theirbrood decreased their response with an artificial reductionin brood size much less. Because the owl used poses a seriousrisk to the defenders, as compared to the woodpecker, the resultlends powerful support to the "total loss" version of the modelof unshared PI; it predicts brood size to affect unshared PImore strongly when there is less risk to the parent. This interpretationis correct to the extent that one premise of the model, namelythat of uncompromised parentage, can be relaxed; great tit broodscontain a sizeable number of extrapair young. Males defendedtheir brood more strongly than did females. Sex and brood manipulationadded up linearly when affecting defense level, i.e., therewas no interaction.     

Metastaseous adenocarcinoma in the oviduct of a great tit (Parus major L.) preventing laying.

A female Great Tit was found to have an adenocarcinoma preventing the egg cells from reaching the ostium part of the oviduct. Metastases were found in the ovary, along the intestine, and in the pancreas, liver and kidney. The frequency of carcinomas among birds was discussed.     

Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major

A brood manipulation experiment on great tits Parus major was performedto study the effects of nestling age and brood size on parentalcare and offspring survival. Daily energy expenditure (DEE)of females feeding nestlings of 6 and 12 days of age was measuredusing the doubly-labeled water technique. Females adjusted theirbrooding behavior to the age of the young. The data are consistentwith the idea that brooding behavior was determined primarilyby the thermoregulatory requirements of the brood. Female DEEdid not differ with nestling age; when differences in body masswere controlled for, it was lower during the brooding periodthan later. In enlarged broods, both parents showed significantlyhigher rates of food provisioning to the brood. Female DEE wasaffected by brood size manipulation, and it did not level offwith brood size. There was no significant effect of nestlingage on the relation between DEE and manipulation. Birds wereable to raise a larger brood than the natural brood size, althoughlarger broods suffered from increased nestling mortality ratesduring the peak demand period of the nestlings. Offspring conditionat fledging was negatively affected by brood size manipulation,but recruitment rate per brood was positively related to broodsize, suggesting that the optimal brood size exceeds the naturalbrood size in this population.     

Ultraviolet reflectance of plumage for parent-offspring communication in the great tit (Parus major)

Ultraviolet (UV) reflectance has been implicated in mate selection.Yet, in some bird species the plumage of young varies in UVreflectance already in the nest and long before mate choiceand sexual selection come into play. Most birds molt the juvenilebody plumage before reaching sexual maturity, and thus, someconspicuous traits of the juvenile body plumage may rather haveevolved by natural selection, possibly via predation or parentalpreference. This second hypothesis is largely untested and predictsa differential allocation of food between fledging and totalindependence, which is a time period of 2–3 weeks whereoffspring mortality is also highest. Here, we test the predictionthat parents use the individual variation in UV reflectanceamong fledglings for differential food allocation. We manipulatedUV reflectance of the plumage of fledgling great tits Parusmajor by treating chest and cheek feathers with a lotion thateither did or did not contain UV blockers and then recordedfood allocation by parents in an outdoor design simulating postfledgingconditions. The visible spectrum was minimally affected by thistreatment. Females were found to feed UV-reflecting offspringpreferentially, whereas males had no preference. It is the firstevidence showing that the UV reflectance of the feathers ofyoung birds has a signaling function in parent–offspringcommunication and suggests that the UV traits evolved via parentalpreference.     

The design and cross-population application of a genome-wide SNP chip for the great tit Parus major

The vast amount of phenotypic information collected in some wild animal populations makes them extremely valuable for unravelling the genetics of ecologically important traits and understanding how populations adapt to changes in their environment. Next generation sequencing has revolutionized the development of large marker panels in species previously lacking genomic resources. In this study, a unique genomics toolkit was developed for the great tit (Parus major), a model species in ecology and behavioural biology. This toolkit consists of nearly 100,000 SNPs, over 250 million nucleotides of assembled genomic DNA and more than 80 million nucleotides of assembled expressed sequences. A SNP chip with 9193 SNP markers expected to be spaced evenly along the great tit genome was used to genotype 4702 birds from two of the most intensively studied natural vertebrate populations [Wytham Woods/Bagley Woods (United Kingdom) and de Hoge Veluwe/Westerheide (The Netherlands)]. We show that (i) SNPs identified in either of the two populations have a high genotyping success in the other population, (ii) the minor allele frequencies of the SNPs are highly correlated between the two populations and (iii) despite this high correlation, a large number of SNPs display significant differentiation (F(ST) ) between the populations, with an overrepresentation of genes involved in cardiovascular development close to these SNPs. The developed resources provide the basis for unravelling the genetics of important traits in many long-term studies of great tits. More generally, the protocols and pitfalls encountered will be of use for those developing similar resources.     

Influence of temperatures during the nestling period on post-fledging survival of great tit Parus major in a Mediterranean habitat

Survival during the first year is one of the most important factors determining fitness in birds. Birds have poor thermoregulatory abilities during the nestling period when the plumage is not fully developed, thus temperature during the nestling period is a serious candidate to affect post-fledging survival, although it has been usually ignored in previous studies. We analysed the relationship between temperatures and post-fledging survival in a great tit Parus major population in Sagunto (Spain) using capture-recapture data from 12 years. Hatching dates, mass at fledging and temperatures during the nestling period (maximum, minimum and mean ambient temperatures as an estimation of the mean and extreme weather conditions that chicks encountered at the nest) were used as individual covariates. Mean post-fledging survival was 0.13±0.01. Adult survival probability was 0.64±0.02. Multi-model inference suggested that post-fledging survival increased with fledging mass, and decreased as temperatures increased. Furthermore, the effect of mass on survival was less important as temperature was higher. We consider that high temperatures affect nestlings' health due to low thermoregulatory abilities of nestlings. Model selection did not support a relationship between hatching dates and survival once mass and temperatures were taken into account. The results suggest the possibility that the effect of date on post-fledging survival found in previous studies was, at least in part, a consequence of the seasonal pattern of temperature variation.