Assessing the Effects of Climate on Host-Parasite Interactions: A Comparative Study of European Birds and Their Parasites

[Background] Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. [Methodology/Principal Finding] Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5–15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5–15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. [Conclusions/Significance] Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5–15 years was used, suggesting that short intervals may bias findings.The Academy of Finland is acknowledged for a grant to TE (project 8119367) and EK (project 250709). PLP was supported by a research grant (TE_291/2010) offered by the Romanian Ministry of Education and Science. T. Szép received funding from OTKA K69068 and JT from OTKA 75618. JMP was supported by a JAE grant from Consejo Superior de Investigaciones Científicas. SM-JM, FdL-AM, JF, JJS and FV were respectively supported by projects CGL2009-09439, CGL2012-36665, CGL2009- 11445, CGL2010-19233-C03-01 and CGL2008-00562 by the Spanish Ministry of Science and Innovation and FEDER and project EVITAR by the Spanish Ministry of Health. FV was also supported by the European Regional Development Fund. MACT was funded by a predoctoral FPU grant from the Spanish Ministry of Education (AP20043713). PM was supported by grant from the Polish Ministry of Science and Higher Education (project 2P04F07030), and the Foundation for Polish Science

Interacciones ecológicas aves-bacterias: implicaciones durante el desarrollo de los pollos en el nido

Tesis inédita de la Universidad Complutense de Madrid, Facultad de Ciencias Biológicas, leída el 28-03-2014Fac. de Ciencias BiológicasTRUEunpu

A spring cold snap is followed by an extreme reproductive failure event in a mountain population of Pied Flycatchers Ficedula hypoleuca

Capsule Very low and anomalous temperatures in early spring of 2010 were followed by the only massive reproductive failure event recorded in 24 years in a population of Pied Flycatchers Ficedula hypoleuca breeding at 1200m altitude in central Spain.Aim To estimate the effects of an extreme climatic event on reproductive success in a montane population of a long-distance migratory bird.Methods We compared nestling growth and mortality in nests of different brood sizes in the context of a brood manipulation experiment.Results Total failure affected 36% of the broods and only 2.5 nestlings on average were raised to fledging age. Most mortality affected broods in the second week of nestling life. Fledglings attained very low values for mass and wing length compared with long-term averages. Subsequent local recruitment was the lowest for any cohort in 24 years. The typical date-dependent decrease in breeding success in the population was inverted.Conclusion Breeding success was markedly affected by a weather event happening one month before hatching and lasting only a few days. An increased frequency of extreme weather events as predicted by some climate change scenarios may dramatically affect insectivorous avian populations in the future.Peer Reviewe

Bacterial degradability of an intrafeather unmelanized ornament: A role for feather-degrading bacteria in sexual selection?

The impact of feather-degrading bacilli on feathers depends on the presence or absence of melanin. Invitro studies have demonstrated that unmelanized (white) feathers are more degradable by bacteria than melanized (dark) ones. However, no previous study has looked at the possible effect of feather-degrading bacilli on the occurrence of patterns of unmelanized patches on otherwise melanized feathers. The pied flycatcher Ficedula hypoleuca Pallas, 1764 is a sexually dimorphic passerine with white wing bands consisting of unmelanized patches on dark flight feathers. These patches are considered to be a sexually selected trait in Ficedula flycatchers, especially in males, where the patches are more conspicuous (larger and possibly whiter) than in females. Using invitro tests of feather bacterial degradation, we compared the degradability of unmelanized and melanized areas of the same feather for 127 primaries collected from the same number of individuals in a population breeding in central Spain (58 males and 69 females). In addition, we also looked for sex differences in feather degradability. Based on honest signalling theory and on the fact that there is stronger sexual selection for males to signal feather quality than in females, we predicted that unmelanized areas should be more degradable by bacteria than melanized ones within the same feather, and that these unmelanized areas should also be more degradable in males than in females. We confirmed both predictions. Microstructural differences between cross-section dimensions of unmelanized and melanized barbs, but not differences in the density of barbs within unmelanized and melanized areas of feathers in males and females, could partly explain differences in degradability. This is the first study to show differences in bacterial degradability among markings on the same feather and among unmelanized feather patches between males and females as predicted by sexual selection theory.This study was funded by projects CGL2007-61251/BOS and CGL2010-19233-C03-02 to JM from the Spanish Ministry of Science and Innovation. SGB and RRC were supported by grants FPI-MEC and JAE-CSIC, respectively.Peer Reviewe

Dietary carotenoid supplementation facilitates egg laying in a wild passerine

During egg laying, females face a trade-off between self-maintenance and investment into current reproduction, since providing eggs with resources is energetically demanding, in particular if females lay one egg per day. However, the costs of egg laying not only relate to energetic requirements, but also depend on the availability of specific resources that are vital for egg production and embryonic development. One of these compounds are carotenoids, pigments with immuno-stimulatory properties, which are crucial during embryonic development. In this study, we explore how carotenoid availability alleviates this trade-off and facilitates egg laying in a small bird species, the blue tit (Cyanistes caeruleus). Blue tits have among the largest clutch size of all European passerines and they usually lay one egg per day, although laying interruptions are frequent. We performed a lutein supplementation experiment and measured potential consequences for egg laying capacity and egg quality. We found that lutein-supplemented females had less laying interruptions and thus completed their clutch faster than control females. No effects of treatment were found on the onset of egg laying or clutch size. Experimentally enhanced carotenoid availability did not elevate yolk carotenoid levels or egg mass, but negatively affected eggshell thickness. Our results provide hence evidence on the limiting role of carotenoids during egg laying. However, the benefits of laying faster following lutein supplementation were counterbalanced by a lower accumulation of calcium in the eggshell. Thus, even though single components may constrain egg laying, it is the combined availability of a range of different resources which ultimately determines egg quality and thus embryonic development.The study was financed by the Ministerio de Economía y Competitividad MINECO, Spain (project CGL2016‐79390‐P to J. Morales) and the European Regional Development Fund (FEDER). J. García‐Campa was supported by FPI grant (BES‐2017‐079750) and J. Morales by a Ramón y Cajal contract from MINECO

Dietary carotenoid supplementation facilitates egg laying in a wild passerine

During egg laying, females face a trade-off between self-maintenance and investment into current reproduction, since providing eggs with resources is energetically demanding, in particular if females lay one egg per day. However, the costs of egg laying not only relate to energetic requirements, but also depend on the availability of specific resources that are vital for egg production and embryonic development. One of these compounds are carotenoids, pigments with immuno-stimulatory properties, which are crucial during embryonic development. In this study, we explore how carotenoid availability alleviates this trade-off and facilitates egg laying in a small bird species, the blue tit (Cyanistes caeruleus). Blue tits have among the largest clutch size of all European passerines and they usually lay one egg per day, although laying interruptions are frequent. We performed a lutein supplementation experiment and measured potential consequences for egg laying capacity and egg quality. We found that lutein-supplemented females had less laying interruptions and thus completed their clutch faster than control females. No effects of treatment were found on the onset of egg laying or clutch size. Experimentally enhanced carotenoid availability did not elevate yolk carotenoid levels or egg mass, but negatively affected eggshell thickness. Our results provide hence evidence on the limiting role of carotenoids during egg laying. However, the benefits of laying faster following lutein supplementation were counterbalanced by a lower accumulation of calcium in the eggshell. Thus, even though single components may constrain egg laying, it is the combined availability of a range of different resources which ultimately determines egg quality and thus embryonic development.The study was financed by the Ministerio de Economía y Competitividad MINECO, Spain (project CGL2016‐79390‐P to J. Morales) and the European Regional Development Fund (FEDER). J. García‐Campa was supported by FPI grant (BES‐2017‐079750) and J. Morales by a Ramón y Cajal contract from MINECO

Sólo algunas poblaciones de ectoparásitos resultan afectadas por la reutilización de nidos: un estudio experimental con papamoscas cerrojillos

The chapter I 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 ; González-Braojos, Sonia; Ruiz-De-Castañeda, Rafael; Moreno Klemming, Juan. Only some ectoparasite populations are affected by nest reuse: an experimental study on pied flycatchers. Ardeola: revista ibérica de ornitología 59(2): 253-266 (2012). https://doi.org/10.13157/arla.59.2.2012.253. http://hdl.handle.net/10261/156381El capítulo I 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 ; González-Braojos, Sonia; Ruiz-De-Castañeda, Rafael; Moreno Klemming, Juan. Only some ectoparasite populations are affected by nest reuse: an experimental study on pied flycatchers. Ardeola: revista ibérica de ornitología 59(2): 253-266 (2012). https://doi.org/10.13157/arla.59.2.2012.253. http://hdl.handle.net/10261/156381[EN] Nest re-use in birds is rare but since appropriate cavities may be scarce, cavity-nesting birds may often re-use those that were occupied in previous seasons. Old nest material may contain and/or attract more ectoparasites than fresh material. Therefore it is important to understand the effects of nest re-use on the abundance of different ectoparasite species of different virulence and their impli cation for breeding parameters and nestling condition. We studied the consequences of nest re-use in a population of pied flycatchers Ficedula hypoleuca breeding in central Spain by offering them both nest-boxes with old nest material and cleaned nest-boxes. We monitored breeding activity from the early stages of nest construction until fledging, and then finally removed nests to estimate ectoparasite abun dances. Occupation rates were similar for both treatments. We found that blowfly and flea abundances were significantly higher in old nests than in new nests, but the abundance of mites, the most virulent ectoparasites on our host study population, was not affected by the presence of old nest material. Nestling growth with respect to tarsus length and mass was not affected by nest re-use although wing length was marginally and significantly reduced by nest re-use. There was no association between ectoparasite abundance and nestling growth and condition. These results question the generality of assumed higher infestations in re-used nests, on which a certain critique of nest-box studies has been based.[ES] La reutilización de nidos en aves es poco común, sin embargo las cavidades más apro piadas para la cría pueden ser escasas, por lo que aves trogloditas, a menudo, pueden volver a ocupar las que utilizaron en temporadas anteriores conteniendo nidos viejos. Debido a que el material de los nidos antiguos puede contener y/o atraer a más ectoparásitos que el material fresco, es importante conocer el efecto que tiene la reutilización de los nidos sobre la abundancia de las distintas especies de ectoparási tos con diferentes virulencias y su implicación sobre los parámetros de reproducción y sobre la condi ción de los pollos. Se han estudiado las implicaciones de la reutilización de los nidos en una población reproductora de papamoscas cerrojillo Ficedula hypoleuca del centro de España, ofreciéndoles para anidar cajas nido con material viejo y cajas nido limpias. Hemos seguido la actividad de cría desde las primeras etapas de la construcción del nido hasta el vuelo de los pollos, siendo los nidos posteriormen te retirados para estimar la abundancia de ectoparásitos. Las tasas de ocupación fueron similares para ambos tratamientos. Hemos encontrado que la abundancia de moscas hematófagas y pulgas son signi ficativamente mayores en nidos con material viejo que en nuevos, pero la abundancia de ácaros, los ectoparásitos más virulentos de nuestra población hospedadora de estudio, no se han visto afectados por la presencia de material viejo en el nido. El crecimiento de los pollos con respecto a la longitud del tarso y al peso no se vio afectado por la reutilización de los nidos, aunque la longitud del ala estuvo marginalmente y negativamente afectada por la reutilización de nido. No hubo asociación entre la abundancia de ectoparásitos y el tamaño y la condición de los pollos. Estos resultados cuestionan la ge neralización de que existen mayores infestaciones en nidos con material viejo en la que se han basado ciertas críticas a la utilización de cajas nido en estos estudios.Peer Reviewe

Extra-Pair Paternity Declines with Female Age and Wing Length in the Pied Flycatcher

Received: November 24, 2014; Initial acceptance: December 17, 2014; Final acceptance: January 13, 2015Despite many studies of how male characteristics affect paternity in predominantly monogamous birds, relatively little attention has been given to the traits of females that may influence extra-pair paternity (EPP). However, the occurrence of EPP may be the result of behavioural interactions in which both male and female traits are important for determining the outcome. If EPP is driven mainly by female choice of extra-pair sires, older, more experienced or larger females would be better able to evade mate guarding tactics and more capable of selecting extra-pair mates and resisting unwanted suitors. This would be especially noticeable in females paired with unattractive mates. On the other hand, if EPP is driven mainly by male pursuit, we should expect that young, inexperienced or small females would be more exposed to coercive male approaches independently of social mate traits. In a study of an Iberian population of the pied flycatcher Ficedula hypoleuca, we found that EPP affected 38% of the broods and 17% of the nestlings. These values are relatively high, allowing a relatively large number of affected within-pair mates to be included. We found that EPP is related to both female and male traits although not to any interaction between male and female traits. EPP was higher at nests tended by both younger and short-winged females and by browner males. Older females may be more experienced and dominant while long-winged females may be faster fliers, these traits enabling them to avoid extra-pair copulations, while brown males are less aggressive towards male intruders. In our study population, EPP appears to be caused by male pursuit, which in some cases may overwhelm female attempts to avoid extra-pair copulations and their social partner's ability to prevent them.The study was ethically approved by the Ethical Committee of CSIC (Spanish Research Council).At the time of the field study, RRdC was supported by a grant from CSIC, and SGB was supported by a contract grant from Ministerio de Ciencia e Innovación.The study has received financial support from projects CGL2010-19233-C03-02 and CGL2013-48193-C3-3-P to JM (DGI-Ministerio de Ciencia e Innovación).Peer reviewe

Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment

The chapter III 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, L.; Palma, Antonio; Alonso-Alvarez, Carlos; González-Braojos, Sonia; Moreno Klemming, Juan. Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment. Oecologia 179(1): 29-41 (2015). http://dx.doi.org/ 10.1007/s00442-015-3321-7. http://hdl.handle.net/10261/156386El capítulo III 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, L.; Palma, Antonio; Alonso-Alvarez, Carlos; González-Braojos, Sonia; Moreno Klemming, Juan. Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment. Oecologia 179(1): 29-41 (2015). http://dx.doi.org/ 10.1007/s00442-015-3321-7. http://hdl.handle.net/10261/156386© 2015, Springer-Verlag Berlin Heidelberg. Ectoparasites may imply a cost in terms of oxidative stress provoked by inflammatory responses in hosts. Ectoparasites may also result in costs for nestlings and brooding females because of the direct loss of nutrients and reduced metabolic capacity resulting from parasite feeding activities. These responses may involve the production of reactive oxygen and nitrogen species that may induce oxidative damage in host tissues. Our goal was to examine the effect of ectoparasites in terms of oxidative stress for nestlings and adult females in a population of pied flycatchers Ficedula hypoleuca. We manipulated the entire nest ectoparasite community by reducing ectoparasite loads in some nests through a heating treatment and compared them with a control group of nests with natural loads. A marker of total antioxidant capacity (TAS) in plasma and total levels of glutathione (tGSH) in red blood cells as well as a marker of oxidative damage in plasma lipids (malondialdehyde; MDA) were assessed simultaneously. Levels of tGSH were higher in heat-treated nests than in controls for both females and nestlings. Higher TAS values were observed in females from heat-treated nests. In nestlings there was a negative correlation between TAS and MDA. Our study supports the hypothesis that ectoparasites expose cavity-nesting birds to an oxidative challenge. This could be paid for in the long term, ultimately compromising individual fitness.This study was financed by project CGL2010-19233-C03-02 to J. M. from the Spanish Ministerio de Ciencia e Innovación (MICINN). P.-R. was supported by a postdoctoral contract from the Spanish Ministerio de Economía y Competitividad (MINECO), through the Severo Ochoa Programme for Centres of Excellence in R&D&I (SEV-2012-0262).Peer Reviewe