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.     

Experimental evidence for density dependence of reproduction in great tits

1. Density dependence of avian reproduction has often been analysed using correlations between annual mean reproductive output and population density. Experiments are necessary to prove that density is the cause of the observed patterns, but so far, three out of four experimental studies do not support a direct causal effect of density on reproduction.
2. This paper presents experimental evidence that reproductive decisions in great tits, Parus major L., are causally affected by breeding density. The breeding density of great tits was manipulated by providing nest-boxes at different densities in an ecologically homogeneous area.
3. Within years the densities in the high and low density plots differed approximately 8-fold. During the 11 years of the experiment, clutch size, nestling mass and the proportion of birds starting a second brood were all lower in the high density plot. In 5 years with equal breeding densities in both parts, clutch size did not differ between the plots. The patterns found were consistent with the density effects as predicted from the non-experimental data.     

Clutch size and malarial parasites in female great tits

life-history models predict an evolutionary trade-off in theallocation of resources to current versus future reproduction.This corresponds, at the physiological level, to a trade-offin the allocation of resources to current reproduction or tothe immune system, which will enhance survival and thereforefuture reproduction. For clutch size, life-history models predicta positive correlation between current investment in eggs andthe subsequent parasite load. In a population of great tits,we analyzed the correlation between natural clutch size of femalesand the subsequent prevalence of Plasmodium spp., a potentiallyharmful blood parasite. Females that showed, 14 days after hatchingof the nestlings, an infection with Plasmodium had a significantlylarger clutch (9.3 eggs ± 0.5 SE, n = 18) than uninfectedfemales (8.0 eggs ± 0.2 SE, n = 80), as predicted bythe allocation trade-off. Clutch size was positively correlatedwith the prevalence of Plasmodium, but brood size 14 days afterhatching was not. This suggests that females incur higher costsduring laying the clutch than during rearing nestlings. Infectionstatus of some females changed between years, and these changeswere significantly correlated with a change in clutch size aspredicted by the trade-off. The link between reproductive effortand parasitism may represent a possible mechanism by which thecost of egg production is mediated into future survival andmay thereby be an important selective force in the shaping ofclutch size     

Is clutch size individually optimized?

Brood size manipulations were carried out to test whether clutchsizevariation in individual great tits (Parus major) controlledforlaying date was tuned to their phenotypic quality and/orlocal food abundance(individual optimization hypothesis; IOH).Broods with different originalclutch sizes, but equal hatchingdates, were manipulated to a common broodsize. A third broodwas kept as a control. Under the IOH, we expected apositiveassociation between reproductive success and original clutchsize.Fledgling production varied in an inconclusive way aftermanipulation, withdata from 1 out of 3 years favoring the IOH.The effect of manipulation on theprobability of a second clutchwas consistent with the IOH in another 1 out ofthe 3 years.When fitness accrued to second broods was also taken intoconsiderationin terms of annual fledgling production, results from 2 outof 3years tended to support the IOH. There was no effect ofthe manipulation onfitness (estimated as the number of recruitsplus parents breeding in the nextseason). Both the clutch component(local recruitment) and the parentalcomponent (survival tillnext breeding season) varied inconclusively withrespect tothe IOH. On the basis of fitness measurements, the IOH couldnot beconfirmed as an explanation for clutch size variationin this population. In 2out of 3 years one of the three fitnesscomponents measured varied inaccordance with the IOH. Overallthe evidence for the IOH in this data set istherefore weak.     

Brood size, sibling competition, and the cost of begging in great tits (Parus major)

Evolutionary theory of parent-offspring conflict explains beggingdisplays of nestling birds as selfish attempts to influenceparental food allocation. Models predict that this conflictmay be resolved by honest signaling of offspring need to parents,or by competition among nestmates, leading to escalated beggingscrambles. Although the former type of models has been qualitativelysupported by experimental studies, the potential for a beggingcomponent driven by scramble competition cannot be excludedby the evidence. In a brood-size manipulation experiment withgreat tits, Parus major, we explored the scramble componentin the begging activity of great tit nestlings by investigatingthe mechanisms of sibling competition in relation to brood size.While under full parental compensation, the feeding rate pernestling will remain constant over all brood sizes for bothtypes of models; the scramble begging models alone predict anincrease in begging intensity with brood size, if begging costsdo not arise exclusively through predation. Great tit parentsadjusted feeding rates to brood size and fed nestlings at similarrates and with similar prey sizes in all three brood-size categories.Despite full parental compensation, the begging and food solicitationactivities increased with experimental brood size, whereas nestlingbody condition deteriorated. These findings support a scramblecomponent in begging and suggest that the competition-inducedcosts of food solicitation behavior play an important role inthe evolution of parent-offspring communication.     

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     

Population density, body size, and phenotypic plasticity of brood size in a burying beetle

Theory predicts that organisms living in heterogeneous environmentswill exhibit phenotypic plasticity. One trait that may be particularlyimportant in this context is the clutch or brood size becauseit is simultaneously a maternal and offspring characteristic.In this paper, I test the hypothesis that the burying beetle,Nicrophorus orbicollis, adjusts brood size, in part, in anticipationof the reproductive environment of its adult offspring. N. orbicollisuse a small vertebrate carcass as a food resource for theiryoung. Both parents provide parental care and actively regulatebrood size through filial cannibalism. The result is a positivecorrelation between brood size and carcass size. Adult bodysize is an important determinant of reproductive success forboth sexes, but only at higher population densities. I testthree predictions generated by the hypothesis that beetles adjustbrood size in response to population density. First, averageadult body size should vary positively with population density.Second, brood size on a given-sized carcass should be larger(producing more but smaller young) in low-density populationsthan in high-density populations. Third, females should respondadaptively to changes in local population density by producinglarger broods when population density is low and small broodswhen population density is high. All three predictions weresupported using a combination of field and laboratory experiments.These results (1) show that brood size is a phenotypically plastictrait and (2) support the idea that brood size decisions arean intergenerational phenomenon that varies with the anticipatedcompetitive environment of the offspring.     

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.     

Latitudinal variation in parental energy expenditure during brood rearing in the great tit

The variation in time and energy allocation of female great tits, Parus major, was studied in five different European populations across a latitudinal gradient. Daily energy expenditure (DEE) was measured in females tending 12-day-old broods. The number of daylight hours used by the parents to collect food for the brood increased with latitude, while DEE and feeding rate per brood tended to level off with latitude. Individual variation in DEE could be explained by variation in ambient temperature (–), the duration of activity period (+) and area, but not by brood size, female body mass, brood mass or feeding rate. When the effect of ambient temperature and the duration of the activity period on the day of energy expenditure measurements were controlled for, female DEE still tended to level off with latitude. Temperature and activity alone can thus not explain the observed pattern. The present study suggests that parents at southern latitudes may be under a time constraint and do not increase energy expenditure because they have no more daylight hours available for foraging, while birds at northern latitudes may be under an energy constraint because they do not make full use of the long daylight period available. Received: 25 May 1999 / Accepted: 08 September 1999     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

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.     

Differential response by males and females to manipulation of partner contribution in the great tit (Parus major)

1.  In birds with bi-parental care, handicapping is often assumed to decrease the amount of parental care of the handicapped partner. We discuss how handicapping could alter the shape of the handicapped bird's survival–effort curve (theoretical curve relating the survival of a parent to its effort) and show that the optimal response could yield a decrease, no response or even an increase in effort of the handicapped bird.
2.  Male or female great tits Parus major (L.) were handicapped during the nestling period by clipping a number of feathers in order to study the effects on parental care and body condition.
3.  Handicapped males significantly decreased their feeding rates, while handicapped females did not. Condition of handicapped females significantly deteriorated, while condition of handicapped males did not change during the experiment. Females with a handicapped partner fully compensated for their partner's decrease in work rate, while males with a handicapped partner did not show any compensation and even tended to decrease their feeding rates.
4.  Using an inverse optimality approach, we reconstructed the theoretical curve relating the survival of a parent to its effort on the basis of the experimental effects. The handicapped male's survival–effort curve appeared to be slightly steeper than that of handicapped females. This suggests that handicapped males suffer more from an increase in effort than handicapped females.     

Reproductive investment and parasite susceptibility in the Great Tit

1. Reproduction and parasite defence are assumed to be costly activities for hosts, and therefore trade-offs might exist between reproduction and parasite defence.
2. Brood sizes were manipulated in a population of Great Tits ( Parus major L.) to assess trade-offs between reproduction and parasite defence. Blood samples were taken from males and females during the late nestling phase, and parasite prevalence was compared among parents raising enlarged, reduced and control broods.
3. A higher prevalence of protozoan blood parasites dominated by Haemoproteus majoris was found among parents with enlarged broods, as compared with parents with control and reduced broods, respectively. Brood size manipulation did not affect parasite prevalence between the sexes or between age classes differently.
4. Mean parasite intensity (number of parasites per microscope field) among adult birds only infected with H. majoris was higher for parents with experimentally enlarged broods than controls and reduced broods, respectively.
5. These results support the hypothesis of a trade-off between parasite defence and reproduction.     

Inbreeding depression along a life-history continuum in the great tit

Inbreeding resulting from the mating of two related individuals can reduce the fitness of their progeny. However, quantifying inbreeding depression in wild populations is challenging, requiring large sample sizes, detailed knowledge of life histories and study over many generations. Here we report analyses of the effects of close inbreeding, based on observations of mating between relatives, in a large, free-living noninsular great tit (Parus major) population monitored over 41 years. Although mating between close relatives (f > or = 0.125) was rare (1.0-2.6% of matings, depending on data set restrictiveness), we found pronounced inbreeding depression, which translated into reduced hatching success, fledging success, recruitment to the breeding population and production of grand offspring. An inbred mating at f = 0.25 had a 39% reduction in fitness relative to that of an outbred nest, when calculated in terms of recruitment success, and a 55% reduction in the number of fledged grand offspring. Our data show that inbreeding depression acts independently at each life-history stage in this population, and hence suggest that estimates of the fitness costs of inbreeding must focus on the entire life cycle.     

Climate change and breeding parameters of great and blue tits throughout the western Palaearctic

Increasing evidence suggests that climate change has consequences on avian breeding phenology. Here, variations in laying date and clutch size of great tit Parus major and blue tit Parus caeruleus within and between breeding populations through the western Palaearctic are examined in relation to climatic fluctuations, measured by the winter North Atlantic Oscillation (NAO) index. Within and across breeding sites, laying date was related to winter‐NAO index such that great and blue tit females lay earlier after warmer, moister winters (positive values of winter NAO‐index). The present study shows that for most populations there is an advancement of laying date, but the rate of change with respect to NAO significantly differed geographically across the western Palaearctic and did not differ between species. However, clutch size of great and blue tits was not affected by climatic fluctuations, presumably because the whole season is being shifted, but not in relation to food supplies. These combined analyses for the two species controlled for potentially confounding variables such as latitude, longitude, elevation and habitat of each study site.     

The evolution of egg size in the brood parasitic cuckoos

We compared genera of nonparasitic cuckoos and two groups ofparasitic cuckoos: those raised together with host young ("nonejectors")and those in which the newly hatched cuckoo either ejects thehost eggs or chicks, or kills the host young ("ejectors"). Nonejectorsare similar to their hosts in body size and parasitize largerhosts than do ejectors, which parasitize hosts much smallerthan themselves. In both types of parasite, the cuckoo's eggtends to match the host eggs in size. To achieve this, nonejectorshave evolved a smaller egg for their body size than have nonparasiticcuckoos, and ejectors have evolved an even smaller egg. Amongejector cuckoo genera, larger cuckoos have larger eggs relativeto the eggs of their hosts, and the relationship between cuckooegg volume (mass of the newly-hatched cuckoo) and host egg volume(mass to be ejected) did not differ from that predicted by weight-liftingallometry. However, comparing among Cuculus cuckoo species,the allometric slope differed from the predicted, so it is notclear that egg size is related to the need to give the cuckoochick sufficient strength for ejection. Comparing the two mostspeciose ejector genera, Chrysococcyx cuckoos (smaller and parasitizedome-nesting hosts) lay eggs more similar in size to their host'seggs than do Cuculus cuckoos (larger and parasitize open cup–nestinghosts). Closer size-matching of host eggs in Chrysococcyx mayreflect the following: (1) selection to reduce adult body massto facilitate entry through small domed nest holes to lay, and(2) less need for a large egg, because longer incubation periodsin dome-nesting hosts allow the young cuckoo more time to growbefore it need eject host eggs.