Adaptaciones fisiológicas en el papamoscas cerrojillo (Ficedula hypoleuca): estrés oxidativo, reproducción y desarrollo

Tesis Doctoral inédita leída en la Universidad Autónoma de Madrid, Facultad de Ciencias, Departamento de Ecología. Fecha de lectura: 11-09-2017Esta tesis tiene embargado el acceso al texto completo hasta el 11-03-201

Phenotypic plasticity in breeding plumage signals in both sexes of a migratory bird: responses to breeding conditions

Adaptive phenotypic plasticity may respond to present ambient conditions. Sexual and social signals in both sexes may express phenotype performance. Plumage signals that change discontinuously allow relating discrete variation to previous performance. Both sexes of the pied flycatcher Ficedula hypoleuca present white patches on the wings and on the forehead, which constitute sexual and social signals. Forehead patches are moulted together with body plumage in Africa, while wing patches are partly moulted in Africa and partly in the breeding area soon after breeding. We studied individual inter‐year changes (corrected for regression to the mean) in the size of forehead and wing patches of both sexes in seven years for females or six years for males in two nearby study areas in central Spain. We found that initial signal extent strongly delimits the possible subsequent changes negatively. There is a negative association of male age with forehead patch changes. Cold and rainy springs are associated in females with decreases in both patch areas and vice versa, while no association with climate is observed in male wing patch changes. Cold pre‐breeding conditions predict positive changes in female wing and male forehead patches. Breeding success is positively associated with forehead patch changes in females. Late‐breeding males experience more positive changes in forehead patch size than early‐breeding males. Some of these trends can be explained by variable costs of breeding in certain conditions for subsequent signal production and/or maintenance, while absence of trends in some cases may be explained by sex differences in costs of breeding and interactions with phenotypic quality of breeders.</p

Males respond to female begging signals of need: A handicapping experiment in the pied flycatcher, Ficedula hypoleuca

The 'female nutrition' hypothesis proposes that food provided by males during incubation is an important energy source for females in bird species in which females alone incubate. Females should be able to communicate their needs through begging signals to mates and males may compensate for the energetic limitations of females through their feeding visits, owing to their overlapping reproductive interests. To test whether female begging during incubation is an honest signal of energetic need and whether mates respond to it we experimentally handicapped female pied flycatchers at the beginning of incubation by clipping two primary flight feathers on each wing. Experimental manipulation led females to intensify begging displays arising from condition impairment and males accordingly increased their incubation feeding rates. Female begging intensity explained more than half of the variation in male incubation feeding rate, thereby showing that female nutrition is the main factor explaining male incubation feeding. Moreover, handicapped females consumed a higher proportion of male food deliveries during the first few days after hatching and weighed less at the end of the nestling period than control females. Handicapping had no influence on female incubation behaviour, hatching and breeding success, nestling and male condition or female nestling provisioning. The provisioning rates of males in the late nestling stage were higher in experimental nests. This is the first experimental study showing that males adjust incubation feeding rates to behavioural displays of need by their mates. The ability of females to modify their begging displays according to need may be an important adaptation that allows females to maintain a good energetic condition during incubation. © 2014 The Association for the Study of Animal Behaviour.This study was financed by project CGL2010-19233-C03-02 to J.M. from Spanish MICINN.Peer Reviewe

Oxidative Stress in Early Life: Associations with Sex, Rearing Conditions, and Parental Physiological Traits in Nestling Pied Flycatchers

The chapter IV of the dissertation: López-Arrabé, Jimena. Physiological adaptations in the pied flycatcher (Ficedula hypoleuca): oxidative stress, reproduction and development (2017), reproduces the manuscript of: López-Arrabé, Jimena ; Cantarero, Alejandro ; Pérez-Rodríguez, Lorenzo ; Palma, Antonio; Moreno, Juan. Oxidative Stress in Early Life: Associations with Sex, Rearing Conditions, and Parental Physiological Traits in Nestling Pied Flycatchers. Physiological and Biochemical Zoology, 89(2): 83-92(2016). http://dx.doi.org/10.1086/685476. http://hdl.handle.net/10261/130300El capítulo IV de la tesis doctoral: López-Arrabé, Jimena. Physiological adaptations in the pied flycatcher (Ficedula hypoleuca): oxidative stress, reproduction and development (2017), reproduce la información del artículo: López-Arrabé, Jimena ; Cantarero, Alejandro ; Pérez-Rodríguez, Lorenzo ; Palma, Antonio; Moreno, Juan. Oxidative Stress in Early Life: Associations with Sex, Rearing Conditions, and Parental Physiological Traits in Nestling Pied Flycatchers. Physiological and Biochemical Zoology, 89(2): 83-92(2016). http://dx.doi.org/10.1086/685476. http://hdl.handle.net/10261/130300Conditions experienced during juvenile development can affect the fitness of an organism. During early life, oxidative stress levels can be particularly high as a result of the increased metabolism and the relatively immature antioxidant system of the individual, and this may have medium- and long-term fitness consequences. Here we explore variation in levels of oxidative stress measured during early life in relation to sex, rearing conditions (hatching date and brood size), and parental condition and levels of oxidative markers in a wild population of the pied flycatcher (Ficedula hypoleuca) followed for 2 yr. A marker of total antioxidant status (TAS) in plasma and total levels of glutathione (GSH) in red blood cells, as well as a marker of oxidative damage in plasma lipids (malondialdehyde [MDA]), were assessed simultaneously. Our results show that nestling total GSH levels were associated with parental oxidative status, correlating negatively with maternal MDA and positively with total GSH levels of both parents, with a high estimated heritability. This suggests that parental physiology and genes could be determinants for endogenous components of the antioxidant system of the offspring. Moreover, we found that total GSH levels were higher in female than in male nestlings and that hatching date was positively associated with antioxidant defenses (higher TAS and total GSH levels). These results suggest that different components of oxidative balance are related to a variety of environmental and intrinsic—including parental—influencing factors. Future experimental studies must disentangle the relative contribution of each of these on nestling oxidative status and how the resulting oxidative stress at early phases shape adult phenotype and fitness.Peer reviewe

Sex-specific associations between telomere dynamics and oxidative status in adult and nestling pied flycatchers

Oxidative stress can contribute to an acceleration of telomere erosion, leading to cellular senescence and aging. Increased investment in reproduction is known to accelerate senescence, generally resulting in reduced future reproductive potential and survival. To better understand the role played by oxidative status and telomere dynamics in the conflict between maintenance and reproduction, it is important to determine how these factors are related in parents and their offspring. We investigated the relationship between oxidative status and telomere measurements in pied flycatchers (Ficedula hypoleuca). Total antioxidant status (TAS) in plasma, total levels of glutathione in red blood cells (RBCs), and oxidative damage in plasma lipids (malondialdehyde [MDA]) were assessed in both parents and nestlings. Telomeres were measured in RBCs in adults. Our results showed sex differences in oxidative variables in adults that are likely to be mediated by sex steroids, with testosterone and estrogens increasing and reducing, respectively, the production of reactive oxygen and nitrogen species. We found a negative association between telomere length (TL) and MDA in adults in the previous season. Moreover, TL was positively associated with TAS in females, while telomere shortening (ΔTL) correlated positively with MDA in males in the current year. These associations could be reflecting differences between sexes in reproductive physiology. We found a positive correlation between parental ΔTL and nestling MDA, an example of how parental physiological aging could affect offspring quality in terms of oxidative stress that highlights the constraints imposed by higher rates of ΔTL during reproduction and rearing

Selection of nest site and nesting material in the Eurasian Nuthatch Sitta europaea

Received 16 September 2014; accepted 5 January 2015This chapter II of the dissertation: Behavioural adaptations of cavity nesting birds, de Alejandro Cantarero (2015), http://hdl.handle.net/10261/127524, reproduces entirely the manuscript of: Selection of nest site and nesting material in the Eurasian Nuthatch Sitta europaea. Ardea - Netherlands Ornithologists' Union 103(1): 91-94 (2015).El capítulo II de la tesis doctoral: Behavioural adaptations of cavity nesting birds, de Alejandro Cantarero (2015), http://hdl.handle.net/10261/127524, reproduce íntegramente la información del artículo: Selection of nest site and nesting material in the Eurasian Nuthatch Sitta europaea. Ardea - Netherlands Ornithologists' Union 103(1): 91-94 (2015).The selection of nest sites and nesting material may have important implications for avian reproductive behaviour and performance. Nest construction may involve costs arising from transporting material that may be reduced considerably if nest materials are located close to the nest site. Eurasian Nuthatch Sitta europaea nests in our nest box study area are mainly composed of pine bark flakes or alternatively of strips of bark of the widespread shrub Cistus laurifolius, with variable amounts of mud being used for plastering the entrance. Several small streams run through the area – an oak Quercus pyrenaica forest with a few scattered pines Pinus sylvestris. Here we show that Nuthatches collected pine bark only when nest sites were situated close to pines, used more mud when breeding close to streams and selected nest sites closer to streams than a sympatric species not using mud, the Pied Flycatcher Ficedula hypoleuca. Nuthatches used pine bark only when there was a pine tree less than 100 m away from the nest box and selected Cistus bark when transport distance was greater. We suggest that the selection of nest sites and nest materials in this species may be constrained by the costs of transporting nest material.This study was financed by project CGL2010-19233-C03-02 and CGL2013-48193-C3-3-P to JM from Spanish MICINN.Peer reviewe

Das Ausmaß der weißen Flecken im Gefieder von weiblichen Trauerschnäppern (Ficedula hypoleuca) korreliert negativ mit der Kortikosteronkonzentration in teilweise pigmentfreien Federn

[EN] Sexually and socially selected signals are predicated to express the present and past condition of individuals and thereby their capacity to cope with environmental challenges. The concentration of corticosterone in feathers (CORTf) has been validated as a marker of activation of the hypothalamic-pituitary axis in birds during feather development. Measurements of CORTf can thus express the physiological stress of migratory birds during non-breeding periods of the annual cycle when feathers moulted in the wintering range are analysed. Thus, negative trends of ornament expression with CORTf may be predicted. Unpigmented plumage patches may constitute signals of phenotypic quality and are used in many species in social interac-tions by both sexes. Pied Flycatchers of both sexes Ficedula hypoleuca show white forehead and wing patches during the breeding season, of which the forehead and part of the wing patch (tertials) are moulted on the wintering grounds before spring migration. These patches are used as signals in social and sexual interactions and their expression has been previ-ously related to several indicators of physiological status. We collected tertials of females during nestling provisioning in a Spanish population and determined their CORTf in the laboratory. CORTf was thus measured in some of the prenuptially moulted feathers used as signals of social dominance by breeding females. According to AICc model selection, CORTf turned up in all the best models explaining forehead patch size and in most best models for wing patch size when controlling for age and size. Both forehead and wing patch sizes were negatively related to CORTf, although the trend for wing patch size was not significant. This indicates that breeding females expressing large unpigmented patches experienced low levels of stress during the prenuptial moult in their winter quarters, or that strongly signalling individuals present a lower level of activation of the HPA axis.[AL] Soziale und für das jeweilige Geschlecht selektierte Signale sollen die gegenwärtige und vorangegangene Verfassung von Individuen anzeigen und damit ihre Fähigkeit, mit den Herausforderungen der Umwelt fertigzuwerden. Die Konzentration von Kortikosteron in den Federn (CORTf) wurde bei Vögeln während der Federentwicklung als Marker für die Aktivierung der Hypothalamus-Hypophysen-Achse validiert. Messungen des CORTf können daher den physiologischen Stress von Zugvögeln im Jahreszyklus außerhalb der Brutzeiten ausdrücken, wenn man im Überwinterungsgebiet bei der Mauser aus-gefallene Federn analysiert. Somit können möglicherweise negative Trends im gesamten Federkleid vorhergesagt werden. Unpigmentierte Stellen im Gefieder können Signale der phänotypischen Qualität darstellen und werden bei vielen Arten in sozialen Interaktionen von beiden Geschlechtern verwendet. Trauerschnäpper (Fidecula hypoleuca) beider Geschlechter zeigen während der Brutzeit weiße Stirn- und Flügelflecken; die Federn an Stirn und Teilen der Flügel mausern im Win-terquartier vor Beginn des Frühjahrszuges. Die Flecken werden in sozialen Interaktionen und zwischen den Geschlechtern als Signal eingesetzt, und ihr Ausprägungsgrad wurde bislang mit mehreren Indikatoren für die physiologische Verfassung in Verbindung gebracht. Wir sammelten die Federn von Weibchen einer spanischen Population während des Nestbaus und bestimmten deren CORTf im Labor. Somit wurde CORTf in Federn aus der Mauser vor der Begattung gemessen, die von brütenden Weibchen als Zeichen ihrer sozialen Dominanz benutzt werden. Bei der Prüfung des Alters und der Körpergröße tauchte unter den AICc-Modellen die CORTf zur Erklärung der Größe des Stirnflecks in allen bestgeeigneten Modellen auf, zur Erklärung der Größe der Flügelflecken in den meisten bestgeeigneten Modellen. Die Größe sowohl der Stirn- als auch der Flügelflecken korrelierte negativ mit CORTf, letztere allerdings nicht signifikant. Dies deutet darauf hin, dass brütende Weibchen mit großen pigmentfreien Flecken während der ersten Mauser im Winterquartier einem niedrigen Stresslevel ausgesetzt waren, oder dass starke Signale aussendende Einzeltiere ein niedrigeres Aktivitätsniveau der Hypothalamus-Hypophysen-Achse aufweisen.The study was supported by project CGL2017-83843-C2-1 from Ministerio de Economía, Industria y Competitividad (MINECO, Spanish Government).Peer reviewe

Die Ausprägung männlicher Gefiedersignale bei Trauerschnäppern Ficedula hypoleuca hängt mit der Kortikosteronkonzentration in den Federn zusammen

[EN] Male signals may express the capacity to sustain environmental challenges. In some migratory birds like the Pied Flycatcher Ficedula hypoleuca, plumage ornaments are molted in the winter quarters shortly before spring migration while most feathers are replaced shortly after the breeding season in the breeding areas. The concentration of corticosterone in feathers (CORTf) may relate to baseline CORT levels at the time of molt which could be expressed through plumage signals. Male Pied Flycatchers present white patches on forehead feathers and tertials which are molted before spring migration and on secondaries and primaries replaced after breeding. They also express a variable degree of melanisation of head and back feathers molted in the wintering areas. All these plumage traits have been previously shown to function in social contests and/or mate attraction. Here we have collected tertials on the two wings and two tail feathers, molted in wintering and breeding areas respectively, of males in a Spanish montane population and analysed CORTf in the laboratory with standard enzyme immunoassays. There is no correlation within individuals between CORTf in the two types of feathers, although levels are similar. The size of the forehead patch is negatively associated with CORTf in tail feathers, mainly in small males, while the blackness of head and back is negatively related to CORTf in tertials, mainly in large males. The size of the wing patch composed of patches on feathers molted both in wintering (tertials) and breeding areas (primaries and secondaries) is not related to CORTf in any type of feather. Different male plumage traits thus may reflect circulating CORT levels during molt processes occurring in the wintering respectively breeding range as expressed by CORTf in different types of feathers.[AL] Männliche Signale könnten die Fähigkeit, schwierige Umweltbedingungen auszuhalten, ausdrücken. Bei einigen Zugvögeln, wie dem Trauerschnäpper Ficedula hypoleuca, werden Gefiederornamente im Winterquartier kurz vor dem Frühjahrszug gemausert, während die meisten Federn kurz nach der Brutsaison im Brutgebiet ersetzt werden. Die Konzentration von Kortikosteron in den Federn (CORTf) dürfte mit dem Ausgangs-CORT-Spiegel während der Mauser, der sich in Gefiedersignalen manifestieren könnte, zusammenhängen. Männliche Trauerschnäpper haben weiße Flecken auf den Stirn- und Schirmfedern, die vor dem Frühjahrszug gemausert werden, und auf den Arm- und Handschwingen, die nach der Brut ersetzt werden. Zudem variiert das Ausmaß der Einlagerung von Melanin in die Federn auf Kopf und Rücken, die im Überwinterungsgebiet gemausert werden. Für all diese Gefiedermerkmale ist gezeigt worden, dass sie im sozialen Wettstreit und/oder bei der Anziehung von Partnern eine Rolle spielen. Hier haben wir Schirmfedern von beiden Flügeln und zwei Schwanzfedern, die im Überwinterungs- bzw. Brutgebiet gemausert wurden, von Männchen einer Trauerschnäpperpopulation in einer spanischen Gebirgsregion gesammelt und CORTf im Labor mittels Standard-Enzym-Immunassays analysiert. Bei Individuen gab es keine Korrelation zwischen CORTf in den beiden Federtypen, obwohl die Spiegel ähnlich waren. Die Größe des Stirnflecks war negativ mit CORTf in den Schwanzfedern assoziiert (hauptsächlich bei kleinen Männchen), während die Intensität der Schwarzfärbung von Kopf und Rücken negativ mit CORTf in den Schirmfedern zusammenhing (hauptsächlich bei großen Männchen). Die Größe des Flügelbereichs, der aus Flecken auf Federn besteht, die im Überwinterungsgebiet (Schirmfedern) bzw. im Brutgebiet (Hand- und Armschwingen) gemausert wurden, hing nicht mit CORTf in anderen Federtypen zusammen. Unterschiedliche Gefiedermerkmale der Männchen könnten daher den CORT-Spiegel im Blut während im Überwinterungs- bzw. Brutgebiet ablaufenden Mauserprozessen anzeigen, der sich als CORTf-Spiegel in verschiedenen Federtypen manifestiert.Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature.Peer reviewe

Phenotypic plasticity in breeding plumage signals in both sexes of a migratory bird: responses to breeding conditions

Adaptive phenotypic plasticity may respond to present ambient conditions. Sexual and social signals in both sexes may express phenotype performance. Plumage signals that change discontinuously allow relating discrete variation to previous performance. Both sexes of the pied flycatcher Ficedula hypoleuca present white patches on the wings and on the forehead, which constitute sexual and social signals. Forehead patches are moulted together with body plumage in Africa, while wing patches are partly moulted in Africa and partly in the breeding area soon after breeding. We studied individual inter-year changes (corrected for regression to the mean) in the size of forehead and wing patches of both sexes in seven years for females or six years for males in two nearby study areas in central Spain. We found that initial signal extent strongly delimits the possible subsequent changes negatively. There is a negative association of male age with forehead patch changes. Cold and rainy springs are associated in females with decreases in both patch areas and vice versa, while no association with climate is observed in male wing patch changes. Cold pre-breeding conditions predict positive changes in female wing and male forehead patches. Breeding success is positively associated with forehead patch changes in females. Late-breeding males experience more positive changes in forehead patch size than early-breeding males. Some of these trends can be explained by variable costs of breeding in certain conditions for subsequent signal production and/or maintenance, while absence of trends in some cases may be explained by sex differences in costs of breeding and interactions with phenotypic quality of breeders.Data collection was supported by projects CGL2010-19233-C03-02, CGL2013-48193-C3-3-P and CGL2017-83843-C2-1 to JM from Ministerio de Economía, Industria y Competitividad (MINECO, Spanish Government). AC was funded by a Juan de la Cierva-formación postdoctoral grant (FJCI-2015-23536) from MINECO. JLA and MP were supported by FPI grants from MINECO

Female aggressiveness towards female decoys decreases with mate T level in the pied flycatcher

Social selection is expected to favour the evolution of female aggressive defence of nesting resources in cavity-nesting birds, which may be also mediated by testosterone (T) levels. Male T levels could express male dominance and thereby territorial safety for female partners and thereby reduce their need for aggressive defence. Here, we explored the role of T levels in female-female competition in a songbird, the pied flycatcher Ficedula hypoleuca. In an experiment with female decoys placed close to the nestbox at the end of laying, we explored if female aggressiveness is related to their own T level or to mate T level. T levels of males and females were measured in the middle of the nestling period. Mean female aggressiveness towards decoys in three presentations was estimated through proximity to the decoy and number of attacks by females, two variables which were positively associated. Aggressiveness by female nest owners to female decoys was negatively related to male T level but unrelated to own T level. There was no assortative mating with respect to T level. Female aggressiveness is more strongly related to the hormonal status of mates than to their own.The study has received financial support from project CGL2013-48193-C3-3-P to JM (DGI-Ministerio de Ciencia e Innovación).Peer Reviewe