Plumage Bacterial Assemblages in a Breeding Wild Passerine: Relationships with Ecological Factors and Body Condition

Microorganisms have been shown to play an important role in shaping the life histories of animals, and it has recently been suggested that feather-degrading bacteria influence the trade-off between parental effort and self-preening behavior in birds. We studied a wild breeding population of great tits (Parus major) to explore habitat-, seasonal-, and sex-related variation in feather-degrading and free-living bacteria inhabiting the birds' yellow ventral feathers and to investigate associations with body condition. The density and species richness of bacterial assemblages was studied using flow cytometry and ribosomal intergenic spacer analysis. The density of studied bacteria declined between the nest-building period and the first brood. The number of bacterial phylotypes per bird was higher in coniferous habitat, while bacterial densities were higher in deciduous habitat. Free-living bacterial density was positively correlated with female mass; conversely, there was a negative correlation between attached bacterial density and female mass during the period of peak reproductive effort. Bacterial species richness was sex dependent, with more diverse bacterial assemblages present on males than females. Thus, this study revealed that bacterial assemblages on the feathers of breeding birds are affected both by life history and ecological factors and are related to body condition.     

Ectoparasites and reproductive trade-offs in the barn swallow (Hirundo rustica)

Parents are predicted to trade offspring number and quality against the costs of reproduction. In altricial birds, parasites can mediate these costs because intensity of parasitism may increase with parental effort. In addition, parasites may mediate a trade-off between offspring number and quality because nestlings in large broods may have reduced anti-parasite immune defence. In this study, we experimentally analysed the effect of brood size on infestation by an ectoparasitic mite in nests of barn swallows (Hirundo rustica). Nests with an enlarged brood had larger prevalence and intensity of infestation than those with a reduced brood. Importantly, each nestling in enlarged broods was exposed to a larger number of mites, even when measured on a per nestling basis, than in reduced broods. Nestlings in enlarged broods had smaller body mass and T-cell-mediated immune response compared to reduced broods. T-cell-mediated immune response and feather growth were negatively correlated with per nestling intensity of infestation in enlarged but not in reduced broods. The results suggest that nestlings in enlarged broods have depressed immunity leading to larger per nestling mite infestation. Hence, exposure to parasites of offspring and parents increases with brood size, and parasitism can thus mediate trade-offs between reproduction and number and quality of the progeny in the barn swallow.     

Male eastern bluebirds trade future ornamentation for current reproductive investment

Life-history theory proposes that organisms must trade-off investment in current and future reproduction. Production of ornamental display is an important component of reproductive effort that has rarely been considered in tests of allocation trade-offs. Male eastern bluebirds (Sialia sialis) display brilliant ultraviolet-blue plumage that is correlated with mate acquisition and male competitive ability. To investigate trade-offs between current reproductive effort and the future expression of a sexually selected ornament, we manipulated the parental effort of males by changing their brood sizes. We found that parents provisioned experimentally enlarged broods more often than reduced broods. As predicted by life-history theory, the change in parental effort had a significant effect on the relative plumage ornamentation of males in the subsequent year: males with reduced broods significantly increased in plumage brightness. Moreover, this change in plumage coloration had a direct effect on the timing of breeding in the following season: males that displayed brighter plumage in the year following the manipulation mated with females that initiated egg laying earlier in the season. These data indicate that male bluebirds must trade-off conserving energy for production of future ornamentation versus expending energy for current reproduction.     

Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolor)

We examined whether strategies of reproductive allocation may reduce long-term immunocompetence through the effects of manipulated effort on secondary or acquired immunity. We tested whether increased reproductive effort leads to reduced immune function and survival by manipulating brood size in tree swallows (Tachycineta bicolor) and exposing breeding females to a primary and secondary exposure of sheep red blood cells to elicit a humoral immune response. Females raising enlarged broods produced fewer secondary antibodies than did females raising control or reduced broods. Most importantly, individuals with high secondary responses were more likely to survive to breed 3 years after brood manipulations, suggesting that differences in disease susceptibility may be caused by trade-offs in reproductive allocation. We also found that individual quality, measured by clutch initiation date, mediated the effects of brood manipulations, with higher-quality birds showing a greater ability to deal with increases in effort.     

Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress

Parental effort is usually associated with high metabolism that could lead to an increase in the production of reactive oxidative species giving rise to oxidative stress. Since many antioxidants involved in the resistance to oxidative stress can also enhance immune function, an increase in parental effort may diminish the level of antioxidants otherwise involved in parasite resistance. In the present study, we performed brood size manipulation in a population of great tits (Parus major) to create different levels of parental effort. We measured resistance to oxidative stress and used a newly developed quantitative PCR assay to quantify malarial parasitaemia. We found that males with an enlarged brood had significantly higher level of malarial parasites and lower red blood cell resistance to free radicals than males rearing control and reduced broods. Brood size manipulation did not affect female parasitaemia, although females with an enlarged brood had lower red blood cell resistance than females with control and reduced broods. However, for both sexes, there was no relationship between the level of parasitaemia and resistance to oxidative stress, suggesting a twofold cost of reproduction. Our results thus suggest the presence of two proximate and independent mechanisms for the well-documented trade-off between current reproductive effort and parental survival.     

Experimental dissociation of individual quality, food and timing of breeding effects on double-brooding in a migratory songbird

Annual reproductive success in many species is influenced by the number of breeding attempts within a season. Although previous studies have shown isolated effects of female quality, food, and timing of breeding on the probability of female birds producing second broods, to our knowledge, none have tested the relative importance of multiple factors and their interactions using simultaneous manipulations within populations of free-living birds. In this study, we show that individual quality and timing of breeding interact to affect the probability of double-brooding in female mountain bluebirds (Sialia currucoides). High-quality females (those that naturally initiated clutches early in the season) were more likely to double-brood, regardless of whether their hatching date was advanced or delayed, whereas later breeding, lower quality females were much less likely to double-brood when their first attempt was delayed. This indicates that annual fecundity of poorer quality (or younger) female bluebirds may be more sensitive to seasonal variation in environmental conditions. In addition, birds that were provided with supplemental food throughout first breeding attempts were more likely to double-brood in one of the study years, suggesting that female bluebirds may be energetically limited in their capacity to initiate a second brood. Females that had their first brood delayed also had a shorter inter-brood interval and were moulting fewer feathers during second broods compared to controls, while females in better condition showed more advanced moult in second breeding attempts. Taken together, our results demonstrate the combined effects of age- or individual quality-mediated energetic trade-offs between current and future reproduction, and between investments in offspring and self-maintenance, on annual fecundity of female birds.     

Fitness and feather wear in the Collared Flycatcher Ficedula albicollis

Individual variation in the degree of feather wear is potentially a useful marker of individual quality or fitness, but next to nothing is known about causes and fitness consequences of feather wear in birds. We studied the effects of sex, age, year and experimental manipulation of brood size on primary feather wear in Collared Flycatchers Ficedula albicollis , and related variation in degree of feather wear to differences in fitness (viz. recruitment, survival). At the end of the breeding period, females and young birds had more worn flight feathers than males and adult birds, and the sexual difference in the degree of feather wear was particularly pronounced in one of the two study years. Experimental reduction of brood size reduced the degree of primary feather wear, whereas experimental enlargement of brood size did not lead to increased feather wear. In both sexes, there was a clear tendency for very old (>5 years old) birds to have more worn feathers than middle aged birds. The individual differences in the degree of feather wear were not correlated with individual differences in recruitment rate of young, but survival probability to the next breeding season increased with increasing degree of feather wear.     

Is the small clutch size of a Corsican blue tit population optimal?

In an attempt to test predictions of the optimisation hypothesis of life history traits in birds, we estimated fitness consequences of brood size manipulations. Experiments were carried out over a period of 4 years in a Mediterranean population of blue tits Parus caeruleus which is confronted with a particular set of environmental constraints. Effects of brood size manipulation were investigated in relation to year-to-year variation in environmental conditions, especially caterpillar abundance. There was a strong variation in the effects of brood size manipulation depending on year. Most effects were on offspring quality (fledging mass, tarsus length). The absolute number of recruits did not significantly differ among categories (reduced, control, enlarged broods) but varied considerably among years. Females recruited from enlarged broods were of lower quality, started to breed later and laid fewer eggs than those recruited from control and reduced broods. Neither parental survival nor reproductive performances of adults in year n + 1 was affected by brood size manipulation in year n. Thus there was no evidence for a cost of reproduction in this population. Since the number of recruits did not depend on brood size manipulation (recruitment rates were higher in reduced broods), but recruits from reduced broods were of better quality compared with other groups, we conclude that adults lay a clutch that is larger than that which is predicted by the optimisation hypothesis. Producing more young could incur some penalties because offspring from large broods are of lower quality and less likely to recruit in the population. Two possible reasons why decision rules in this population seem to be suboptimal are discussed. Received: 10 March 1998 / Accepted: 1 July 1998     

Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca

The physiological mechanism underlying the cost of reproduction may consist of immunodepression caused by increased parental effort. Here, we report effects of experimental manipulation of clutch size on T-lymphocyte cell-mediated immune response in female pied flycatchers, Ficedula hypoleuca. Parents with reduced broods provisioned at lower rates than those caring for control and enlarged broods three days after hatching. Parents caring for enlarged broods provisioned nests at higher rates 13 days after chick hatching than those feeding control and reduced broods. Females with enlarged broods weighed less than females with control or reduced broods. No effect of experimental treatment on nestling mass and size was found. The response to the injection of phytohaemagglutinin in the wing-web of females decreased with increasing brood size and with increasing provisioning rate when the chicks were three days old, when controlling for the negative effect of female mass on response. The T-lymphocyte cell-mediated response decreased from the reduced to the control, and from this to the enlarged group, when controlling for female mass. This effect of experimental manipulation of clutch size was significant and consistent with a trade-off between maternal effort and immunocompetence.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling barn swallows Hirundo rustica

We investigate the trade-off between reproductive effort, health status and T-lymphocyte acquired immunity in female and nestling barn swallows Hirundo rustica using a brood size manipulation experiment. Maternal and total feeding effort increased with experimental brood size. Parents did not fully compensate for the increased food demand of the enlarged broods and as a consequence the per capita feeding rate of nestlings decreased with increasing experimental brood size. Body mass and a measure of T-cell mediated immunity in 12 days old nestlings also decreased with increasing experimental brood size. Different leucocyte concentrations and the heterophile/lymphocyte ratio – an index of stress – of nestlings did not change in relation to experimental brood size, suggesting that within brood competition did not affect stress to nestlings. The brood size manipulation had a significant effect on maternal T-cell mediated immunity, measured by the phytohemagglutinin skin test, but not on maternal body mass, haematocrit or differential or total white blood cell counts. Our results seem to support the prediction that under mild work stress females respond first by reducing the energetically expensive acquired immunity. Different leucocyte types and the heterophile/lymphocyte ratio appear less sensitive to parental workload.     

Responses by Central‐Place Foragers to Manipulations of Brood Size: Parent Flickers Respond to Proximate Cues but do not Increase Work Rate

Manipulations of brood size measure the willingness or ability of parents to invest in offspring and different reproductive roles may lead to differences in feeding effort between the sexes. Parental investment in birds is usually assessed by quantifying feeding rates, but this provides an incomplete picture of parental effort because it fails to account for how parents collect food on the landscape. We studied northern flickers (Colaptes auratus), a woodpecker in which males provide the majority of parental care and used a repeated measures design and short‐term (24 h) brood enlargements (N = 35) and reductions (N = 27) to assess effects of treatment on feeding rates to nestlings and parental foraging behaviour. Parents of enlarged broods did not significantly increase feeding rate, resulting in a decline in nestling mass. Parents of reduced broods decreased their feeding rates by 84%, but increased per capita feeding rates, resulting in nestling mass gain. The variation in feeding rates to enlarged broods was not influenced by feather corticosterone, body condition, feather re‐growth rate or mass change between the incubation and nestling periods. Foraging pattern on the landscape remained the same during the enlarged treatment for both sexes. We conclude that flickers respond to proximate cues in brood demands, but do not increase feeding rates to enlarged broods, at least in the short term. A literature review suggested that this lack of response is atypical for short‐lived species. We hypothesize that parents in species with large home ranges and long nestling periods face energetic limitations that constrain their ability to respond to enlarged broods. We encourage future studies to assess foraging behaviour on the landscape to document important trade‐offs for parents such as predation risk and energy expenditure while feeding offspring.     

The effect of brood size and age on partial filial cannibalism in the scissortail sergeant

Within the size range found in the field for the scissortail sergeant Abudefduf sexfasciatus , there was no correlation between the number of cannibalized eggs and total brood size. Very small broods were fully cannibalized. In a manipulation experiment, males were provided with broods of one of three standardized sizes: at the two extremes and in the middle of the range of naturally occurring broods. Brood size had no effect on partial filial cannibalism, but parental effort increased with increasing brood size. Field correlates and the manipulation experiment showed that the cost of cannibalism in terms of current reproductive success decreased significantly with increasing brood size. Contrary to expectations, there was no relationship between male size and the incidence of cannibalism. No preference for younger eggs was found either from field correlates or from a manipulative experiment in which males were provided with an equal number of young and old eggs at the beginning of the parental phase.     

Avian malaria is associated with increased reproductive investment in the blue tit

Haemosporidians causing avian malaria are very common parasites among bird species. Their negative effects have been repeatedly reported in terms of deterioration in survival prospects or reproductive success. However, a positive association between blood parasites and avian fitness has also been reported. Here, we studied a relationship between presence of malaria parasites and reproductive performance of the host, a hole‐breeding passerine – the blue tit Cyanistes caeruleus. Since the malaria parasites might affect their hosts differently depending on environmental conditions, we performed brood size manipulation experiment to differentiate parental reproductive effort and study the potential interaction between infection status and brood rearing conditions on reproductive performance. We found individuals infected with malaria parasites to breed later in the season in comparison with uninfected birds, but no differences were detected in clutch size. Interestingly, infected parents produced heavier and larger offspring with stronger reaction to phytohemagglutinin. More importantly, we found a significant interaction between infection status and brood size manipulation in offspring tarsus length and reaction to phytohemagglutinin: presence of parasites had stronger positive effect among birds caring for experimentally enlarged broods. Our results might be interpreted either in the light of the parasite‐mediated selection or terminal investment hypothesis.     

Serum immunoglobulin G levels are positively related to reproductive performance in a long-lived seabird, the common tern (Sterna hirundo)

The evolution of longevity requires a low risk of mortality from extrinsic factors, relative to intrinsic factors, so that individuals that differentially invest in physiological self-maintenance and minimize their annual reproductive costs will maximize lifetime fitness through a prolonged reproductive lifespan. The trade-off between reproductive effort and self-maintenance, as measured by immune function, has been well documented in short-lived birds, but is difficult to demonstrate in long-lived birds. To assess self-maintenance in a long-lived seabird, we measured serum protein levels, including immunoglobulin G (IgG = IgY), in 30 breeding pairs of common terns (Sterna hirundo) and their first-hatched (A) chicks. Most parents were of known age from banding as hatchlings; our sample was selected to contrast young breeders (6–9 years) with very old birds (17–23 years). Body-mass of the parents declined by 5% during the chick-rearing period, while serum protein levels were stable. Serum IgG levels were higher in parents of offspring with faster growth rates, while IgG levels were lower in parents whose broods were reduced by starvation. A-chicks in broods of two had higher IgG levels than singleton chicks. Albumin levels were not related to reproductive performance. Thus, despite adequate statistical power, we could find no evidence for a trade-off between reproduction and self-maintenance in common terns, even in old age. The results are consistent with life-history predictions for long-lived vertebrates, in which selection favors sustained self-maintenance across the reproductive lifespan. The positive relationships between IgG levels and reproductive performance indicate that IgG can be used as an index of parental “quality.”     

Brood size and immunity costs in zebra finches Taeniopygia guttata

Birds rearing experimentally enlarged broods have lower antibody responses to a novel antigen, and we tested three hypotheses that could explain this result. We used zebra finches Taeniopygia guttata inoculated with sheep red blood cells (SRBC) as a study system, for which this trade-off was previously demonstrated. 1. Compensatory cellular immunity: The humoral immune response is slow, and removal of SRBC through up-regulated cellular immunity could pre-empt an antibody response. However, cellular immune response to PHA decreased with increasing brood size, allowing rejection of this hypothesis. 2. Costs of antibody-production: Chicks in large broods grow less well, and birds with large broods may allocate resources to chicks instead of antibodies when these are costly. Compared to saline controls, SRBC suppressed metabolic rate in the hours following immunisation, but there was no effect in the following night, or at any time 4 and 8 days later. Fitness costs were measured by repeatedly immunising parents with SRBC while rearing young. Chick growth, parental condition, and subsequent reproduction of the parents were not affected by SRBC. We conclude that the costs of antibody formation cannot explain the trade-off between brood size and antibody responsiveness. 3. Costs of immune system maintenance: Maintaining a system enabling antibody-formation may be very costly, and birds rearing large broods may have down-regulated this system. Based on this hypothesis we predicted that antibody formation would still be reduced in parents rearing large broods when immunised after rearing the chicks. Our results confirmed this prediction, and we suggest that birds rearing large broods have lower antibody responses because they economised on the maintenance costs of the immune system.     

A Trade-Off between Reproduction and Feather Growth in the Barn Swallow (Hirundo rustica)

Physiological trade-offs mediated by limiting energy, resources or time constrain the simultaneous expression of major functions and can lead to the evolution of temporal separation between demanding activities. In birds, plumage renewal is a demanding activity, which accomplishes fundamental functions, such as allowing thermal insulation, aerodynamics and socio-sexual signaling. Feather renewal is a very expensive and disabling process, and molt is often partitioned from breeding and migration. However, trade-offs between feather renewal and breeding have been only sparsely studied. In barn swallows (Hirundo rustica) breeding in Italy and undergoing molt during wintering in sub-Saharan Africa, we studied this trade-off by removing a tail feather from a large sample of individuals and analyzing growth bar width, reflecting feather growth rate, and length of the growing replacement feather in relation to the stage in the breeding cycle at removal and clutch size. Growth bar width of females and length of the growing replacement feather of both sexes were smaller when the original feather had been removed after clutch initiation. Importantly, in females both growth bar width and replacement feather length were negatively predicted by clutch size, and more strongly so for large clutches and when feather removal occurred immediately after clutch completion. Hence, we found strong, coherent evidence for a trade-off between reproduction, and laying effort in particular, and the ability to generate new feathers. These results support the hypothesis that the derived condition of molting during wintering in long-distance migrants is maintained by the costs of overlapping breeding and molt.     

Stress,immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation

The two main trade-offs considered determining reproductive patterns in iteroparous organisms are the one between current and future reproduction, and the one between the number and quality of offspring. Recently, it has been suggested that these trade-offs may be mediated by stress-induced reduction in immunocompetence. To test the hypothesis that stress reduces immune function, we investigated the effects of brood size manipulation on stress hormone levels, leukocyte profiles and immune responses against challenge with novel antigens in nestling and parent male pied flycatchers ( Ficedula hypoleuca). In male parents, heterophil (H) and lymphocyte (L) numbers, as well as H/L ratio increased with experimentally enlarged brood size, and corticosterone levels tended to do so, indicating that high parental work load altered their stress level and physiological state. Despite this, we found no effects on humoral immune responsiveness, measured as antibody production against diphtheria-tetanus vaccine. In nestlings, heterophil numbers and H/L ratio increased in enlarged broods, whereas T-cell-mediated immune responsiveness, measured against phytohemagglutinin (PHA), decreased in enlarged broods. The results support the view that growth-stress-induced immunosuppression may be an important physiological pathway mediating the trade-off between the number and viability of offspring. The difference in the observed immune-related responses between nestlings and males may be because we measured different aspects of the immune system (cellular vs humoral). However, it may also be a result of males lowering their own costs by feeding less, (and their mate possibly compensate by feeding more), whereas nestlings cannot escape the costs of increased intra-brood competition.     

Context-dependent effects of parental effort on malaria infection in a wild bird population, and their role in reproductive trade-offs

Although trade-offs between reproductive effort and other fitness components are frequently documented in wild populations, the underlying physiological mechanisms remain poorly understood. Parasitism has been suggested to mediate reproductive trade-offs, yet only a limited number of parasite taxa have been studied, and reproductive effort-induced changes in parasitism are rarely linked to trade-offs observed in the same population. We conducted a brood size manipulation experiment in blue tits (Cyanistes caeruleus) infected with malaria (Plasmodium) parasites, and used quantitative PCR to measure changes in parasitaemia. In one of two years investigated, parasitaemia increased as a result of brood enlargement, and was also positively associated with two other indicators of reproductive effort: clutch size and single parenthood. These associations between both experimental and naturally varying reproductive effort and parasitaemia suggest that immune control of chronic malaria infections can be compromised when parents are working hard. Brood size manipulation significantly affected the number of independent offspring produced, which was maximised when brood size was unchanged. Moreover, when parents were infected with one of two common Plasmodium species, the shape of this trade-off curve was more pronounced, suggesting that parasitic infection may exacerbate the trade-off between quantity and quality of offspring. Although the involvement of parasites in survival costs of reproduction has received much attention, these results suggest their role in other commonly documented reproductive trade-offs, such as that between number and quality of offspring, warrants further study.     

Local sex ratio affects the cost of reproduction

1.?Costs and benefits of reproduction are central to life-history theory, and the outcome of reproductive trade-offs may depend greatly on the ecological conditions in which they are estimated. In this study, we propose that costs and benefits of reproduction are modulated by social effects, and consequently that selection on reproductive rates depends on the social environment. 2.?We tested this hypothesis in a great tit Parus major population. Over 3 years, we altered parental reproductive effort via brood size manipulations (small, intermediate, large) and manipulated the local social environment via changes in the local fledgling density (decreased, increased) and the local sex ratio (female-biased, control, male-biased). 3.?We found that male-biased treatment consistently increased the subsequent local breeding densities over the 3-year study period. We also found that parents rearing small broods in these male-biased plots had increased survival rates compared with the other experimental groups. 4.?We conclude that reproductive costs are the product of an interaction between parental phenotypic quality after reproduction and the social environment: raising a small brood had long-lasting effects on some phenotypic traits of the parents and that this increased their survival chances in male-biased environment where habitat quality may have deteriorated (via increased disease/predation risk or intraspecific competition). 5.?Our results provide the first experimental evidence that local sex ratio can affect reproductive costs and thus optimal clutch size.