Elena Arriero

Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus )

The Hamilton and Zuk hypothesis on haemoparasite–mediated sexual selection and certain studies of reproductive costs are based on the assumption that avian blood parasite infections are detrimental to their hosts. However, there is no experimental evidence demonstrating harmful effects of blood parasites on fitness in wild populations, it even having been suggested that they may be non–pathogenic. Only an experimental manipulation of natural blood parasite loads may reveal their harmful effects. In this field experiment we reduced through medication the intensity of infection by Haemoproteus majoris and the prevalence of infection by Leucocytozoon majoris in blue tits (Parus caeruleus), and demonstrated detrimental effects of natural levels of infection by these common parasite species on host reproductive success and condition. The fact that some of the costs of infection were paid by offspring indicates that blood parasites reduce parental working capacity while feeding nestlings. Medicated females may be able to devote more resources to parental care through being released from the drain imposed upon them by parasites and/or through a reduced allocation to an immune response. Therefore, this work adds support to previous findings relating hosts life–history traits and haematozoan infections.

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.

Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca)

ABSTRACT The number of different types of circulating leucocytes may provide information about the health state of birds in the wild. We counted the number and proportions of circulating leucocytes in blood smears of nestling pied flycatchers (Ficedula hypoleuca) shortly before fledging. We studied the relationship between these haematological measures and environmental factors like parasitism, body mass, hatching date, and brood size. The heterophils-to-lymphocytes ratio was higher in nestlings whose nests suffered from mite infestation and in lighter individuals, heterophils being the cells that responded preferentially to malnutrition. Recruited birds had lower lymphocyte and heterophil counts when nestlings than non-recruited ones. Our results show that heterophil count is a better predictor of local recruitment than other variables widely used for nestlings as survival predictors, like body mass or hatching date, supporting the hypothesis that low heterophil counts reflect a good individual health state in nestlings.

Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds

Abstract Growing altricial birds may experience nutritional stress in the nest due to sibling competition, food restriction, or parasites. Nutritional stress may be detected through its effect on nestling growth, although genetic and maternal effects may interfere with its expression. A more direct way of estimating nutritional stress may be through measurements of organismic stress in growing birds. Heterophil/lymphocyte ratios (H/L) have been proposed as reliable physiological indicators of the stress response. Heat-shock protein (HSP) synthesis is induced by animals in response to various stressors, making the concentration of HSPs a suitable measure of organismic stress. In a study of growing pied flycatchers (Ficedula hypoleuca), we assessed H/L from cell counts in blood smears and levels of two HSPs, HSP60 and HSP70, from the cell fraction of peripheral blood. H/L and the level of HSP60 were significantly positively associated in nestlings of 13 days of age, while the level of HSP70 was not related to the other two measures. Small nestlings with respect to tarsus length on day 7 had higher levels of HSP60 and higher H/L values. Brood means of nestling mass, tarsus length, and wing length shortly before fledging were negatively related to both mean HSP60 level and mean H/L ratio. Brood variances in body mass and wing length on day 13 were positively associated with mean HSP60 levels but not with mean H/L values. Up to 80% of variation in some traits was explained by stress indicators.

Daily energy expenditure and cell-mediated immunity in pied flycatchers while feeding nestlings: interaction with moult

Ecological immunology posits a trade-off between parental effort and immunocompetence underlying the cost of reproduction. The moult-breeding overlap observed in several bird species represents a conflict in resource allocation between two energy-demanding processes. Moult processes have been associated with enlargements of immune system organs. In the present study. we measured simultaneously daily energy expenditure (DEE) and the T-cell-dependent immune response of pied flycatchers, Ficedula hypoleuca, caring for grown nestlings. We used the doubly labelled water technique and the phytohaemagglutinin (PHA) injection assay on both males and females, while recording provisioning rates and moult scores. DEE and the PHA response were negatively correlated for females, but not for males. A significantly higher proportion of males than females initiated moult. Provisioning rates were strongly correlated with DEE for females but only for non-moulting males. The DEE of moulting males was marginally correlated with moult score. For moulting males, there was a marginally significant positive correlation between moult score and immune response. The trade-off between DEE and immunity for females could underlie the cost of reproduction. However, the moult-breeding overlap found in males may offset this trade-off, thereby reducing the implications of immunosuppression for parental survival.

Female hematozoan infection reduces hatching success but not fledging success in Pied Flycatchers Ficedula hypoleuca

Abstract We report association between female blood parasite prevalence (percentage of infected birds) just after egg laying and reproductive success in two successive breeding seasons, in a breeding population of Pied Flycatcher Ficedula hypoleuca in central Spain. Females infected with Trypanosoma spp. had a higher probability of deserting their clutches during the incubation period than noninfected females. Females infected with Haemoproteus balmorali hatched proportionally fewer eggs than noninfected females. Female infected with H. balmorali during the incubation period may have a decreased ability to thermoregulate which may affect their incubation capacity. Fledging success, breeding success, fledgling mass, and tarsus length were not associated with infection of the mother by blood parasites during the incubation period, suggesting that females and their mates may compensate during the nestling period for the negative effect of blood parasites during the incubation period.

Early moult improves local survival and reduces reproductive output in female pied flycatchers

ABSTRACT Overlapping moult and reproduction might be crucial for long-distance migratory birds, which are time-constrained to complete these energy-demanding functions before the onset of migration. However, proximate factors modulating the potential trade-off between moult and breeding, such as haemoparasite infection and stress, have not been studied in wild avian populations. We investigated the occurrence of moult-breeding overlap in females of a Spanish population of pied flycatchers (Ficedula hypoleuca) and its association with female age, haemoparasite prevalences, physiological stress, and condition at initial (incubation phase or beginning of the nestling period) and final breeding stages (days 11–12 of the nestling period). Late-breeding females were more likely to show a moult–breeding overlap than early-breeding females. Female age was not associated with moult status when taking into account laying date and study year. A higher proportion of females infected by Haemoproteus at initial breeding stages showed a moult–breeding overlap. Haemoproteus prevalences at final breeding stages did not differ according to moult status. Females with a moult–breeding overlap also showed better condition and lower stress levels (HSP60 levels) at the end of the season. A higher proportion of moulting females returned to the breeding grounds in the following season compared with non-moulting ones. Conversely, moulting females showed reduced hatching success and numbers of hatchlings and fledglings. Overlapping moult and breeding might be the expression of a shift in resource allocation between present and future reproduction, towards increased self-maintenance and reduced reproductive investment. Nomenclature: Cramp, Perrins & Brooks, 1993.

Habitat structure in Mediterranean deciduous oak forests in relation to reproductive success in the Blue Tit Parus caeruleus

Capsule Effects operate during laying and incubation and with less success in breeding territories characterized by a young and immature vegetation structure. Aims To explore relationships between habitat characteristics at the breeding territory level and reproductive timing and success of Blue Tits Parus caeruleus in Pyrenean Oak Quercus pyrenaica woods in central Spain. Methods Habitat structure of the breeding territories was measured in a sampling plot centred on a nestbox, with a radius of 25 m. A principal component analysis was performed to obtain a factor of ‘territory vegetation maturity’ summarizing the characteristics of the territory. Reproductive parameters were obtained by frequent visits to the nests during the breeding season. Adults were captured at the nest to obtain morphological measurements, and nestling tarsus length and body mass were measured on day 15 after hatching. Results Habitat effects on reproductive performance seem to operate at the beginning of reproduction in these montane oak woods and through female body condition during the first stages of breeding. Female Blue Tits in breeding territories with immature and degraded vegetation started reproduction later and had lower hatching and breeding success. Laying date was strongly related to female body condition. Total reproductive failure occurred mainly during the incubation period and was associated with immature breeding territories. However, nestlings raised in mature forest territories did not differ in size and mass from those in degraded, immature territories. Conclusions The effects of habitat structure on Blue Tit reproductive success operate during laying and incubation in this Mediterranean forest type. The results are discussed in terms of the implications of management of Mediterranean oak woods for the conservation of forest bird populations.

Habitat structure is associated with the expression of carotenoid-based coloration in nestling blue tits Parus caeruleus.

We investigated how the expression of carotenoid-based plumage coloration (lightness and chroma) in nestling blue tits Parus caeruleus is associated with forest structure in oak forests of central Spain. We found evidence of a reduced expression of carotenoid-based coloration in nestlings growing up in successionally young and structurally simple forest territories. Our results suggest that breast feather coloration can be used as an indicator of nestling quality because nestlings with more intense yellow plumage coloration had larger body size and stronger immune responses to the injection of phytohemagglutinin (PHA). Given the association of forest structural complexity with carotenoid-based plumage coloration, our findings suggest that variation in habitat structure may have a significant impact on forest birds in their first stages of life which has implications for forest management practices.

A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature

Long embryonic periods are assumed to reflect slower intrinsic development that are thought to trade off to allow enhanced physiological systems, such as immune function. Yet, the relatively rare studies of this trade-off in avian offspring have not found the expected trade-off. Theory and tests have not taken into account the strong extrinsic effects of temperature on embryonic periods of birds. Here, we show that length of the embryonic period did not explain variation in two measures of immune function when temperature was ignored, based on studies of 34 Passerine species in tropical Venezuela (23 species) and north temperate Arizona (11 species). Variation in immune function was explained when embryonic periods were corrected for average embryonic temperature, in order to better estimate intrinsic rates of development. Immune function of offspring trades off with intrinsic rates of embryonic development once the extrinsic effects of embryonic temperatures are taken into account.