Individual response in body mass and basal metabolism to the risks of predation and starvation in passerines.

Wintering energy management in small passerines has focused on the adaptive regulation of the daily acquisition of energy reserves within a starvation-predation trade-off framework. However, the possibility that the energetic cost of living, i.e. basal metabolic rate (BMR), is being modulated as part of the management energy strategy has been largely neglected. Here, we addressed this possibility by experimentally exposing captive great tits (Parus major) during winter to two consecutive treatments of increased starvation and predation risk for each individual bird. Body mass and BMR were measured prior to and after each week-long treatment. We predicted that birds should be lighter but with a higher metabolic capacity (higher BMR) as a response to increased predation risk, and that birds should increase internal reserves while reducing their cost of living (lower BMR) when exposed to increased starvation risk. Wintering great tits kept a constant body mass independently of a week-long predation or starvation treatment. However, great tits reduced the cost of living (lower BMR) when exposed to the starvation treatment, while BMR remained unaffected by the predation treatment. Energy management in wintering small birds partly relies on BMR regulation, which challenges the current theoretical framework based on body mass regulation.

Prehatching temperatures drive inter-annual cohort differences in great tit metabolism.

Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is, therefore, considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. We studied winter BMR variation of juveniles over a 15-year period in a wild population of great tits Parus major at the northern border of their distribution. BMR during winter consistently changed between years, even after controlling for environmental factors, suggestive of a non-reversible developmental plasticity shaping the adult metabolic phenotype. BMR in cohorts of wintering great tits varied among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Predictability of food supply modulates nocturnal hypothermia in a small passerine.

The combination of short days and long cold winter nights, in temperate regions, presents a major challenge for small diurnal birds. Small birds regularly employ heterothermy and enter rest-phase hypothermia during winter nights to conserve energy. However, we know little about how environmental conditions, such as food availability, shape these strategies. We experimentally manipulated food availability in winter to free-living great tits Parus major. A 'predictable' and constant food supply was provided to birds in one area of a forest, while birds in another area did not have access to a reliable supplementary food source. We found that predictability of food affected the extent of nocturnal hypothermia, but the response differed between the sexes. Whereas male nocturnal body temperature was similar regardless of food availability, females exposed to a naturally 'unpredictable' food supply entered deeper hypothermia at night, compared with females that had access to predictable food and compared with males in both treatment groups. We suggest that this response is likely a consequence of dominance, and subdominant females subject to unpredictable food resources cannot maintain sufficient energy intake, resulting in a higher demand for energy conservation at night.

Mass or pace? Seasonal energy management in wintering boreal passerines.

Research on winter energy management in small vertebrates has focused on the regulation of body mass (BM) within a framework of starvation-predation trade-off. Winter-acclimatized birds exhibit a seasonal increase in both BM and basal metabolic rate (BMR), although the patterns of co-variation between the two traits remain unknown. We studied this co-variation in three different species of wild titmice, great, blue and willow tits, originating from two boreal regions at different latitudes. Seasonal change in BM and BMR was inter-dependent, particularly in the great tit; however, by contrast, no seasonal change was observed in the willow tit. BMR changed non-linearly in concert with BM with a peak in midwinter for both blue and great tits, whereas such non-linear pattern in willow tit was opposite and independent of BM. Surprisingly, BMR appears to be more sensitive to ambient temperatures than BM in all three species studied. Energy management is a multifaceted strategy that cannot be fully understood without considering reserve levels and energy expenditure simultaneously. Thus, our study indicates that the prevailing conceptual framework based on variation in BM alone is insufficient to understand seasonal energy management in small wintering passerines.

Does bird metabolic rate influence mosquito feeding preference?

BACKGROUND: Host selection by mosquitoes plays a central role in the transmission of vector-borne infectious diseases. Although interspecific variation in mosquito attraction has often been reported, the mechanisms underlying intraspecific differences in hosts' attractiveness to mosquitoes are still poorly known. Metabolic rate is related to several physiological parameters used as location cues by mosquitoes, and so potentially affect host-vector contact rates. Therefore, individual hosts with higher metabolic rates should be more attractive to host-seeking mosquitoes. Here, we experimentally investigated the role of bird metabolic rate in the feeding preferences of Culex pipiens (Linnaeus), a widespread mosquito vector of many pathogens affecting human and wildlife health. RESULTS: Passer domesticus (Linnaeus) pairs containing one bird treated with 2,4-dinitrophenol (DNP) and the other injected with phosphate-buffered saline solution (PBS) (i.e. control) were simultaneously exposed overnight to mosquitoes. The treatment did not affect the proportion of mosquitoes biting on each individual. However, mosquito feeding preference was negatively associated with bird resting metabolic rate but positively with bird body mass. These two variables explained up to 62.76% of the variations in mosquito feeding preference. CONCLUSIONS: The relationships between mosquito feeding preferences and individual host characteristics could be explained by enhanced anti-mosquito behaviour associated with higher metabolic rates. The potential role of cues emitted by hosts is also discussed. Thus, individuals with high metabolism may actively avoid being bitten by mosquitoes, despite releasing more attractant cues. Since metabolic rates can be related to individual differences in personality and life history traits, differences in mosquitoes' feeding preferences may be related to intraspecific differences in exposure to vector-borne pathogens.

Different Ultimate Factors Define Timing of Breeding in Two Related Species.

Correct reproductive timing is crucial for fitness. Breeding phenology even in similar species can differ due to different selective pressures on the timing of reproduction. These selection pressures define species' responses to warming springs. The temporal match-mismatch hypothesis suggests that timing of breeding in animals is selected to match with food availability (synchrony). Alternatively, time-dependent breeding success (the date hypothesis) can result from other seasonally deteriorating ecological conditions such as intra- or interspecific competition or predation. We studied the effects of two ultimate factors on the timing of breeding, synchrony and other time-dependent factors (time-dependence), in sympatric populations of two related forest-dwelling passerine species, the great tit (Parus major) and the willow tit (Poecile montanus) by modelling recruitment with long-term capture-recapture data. We hypothesized that these two factors have different relevance for fitness in these species. We found that local recruitment in both species showed quadratic relationships with both time-dependence and synchrony. However, the importance of these factors was markedly different between the studied species. Caterpillar food played a predominant role in predicting the timing of breeding of the great tit. In contrast, for the willow tit time-dependence modelled as timing in relation to conspecifics was more important for local recruitment than synchrony. High caterpillar biomass experienced during the pre- and post-fledging periods increased local recruitment of both species. These contrasting results confirm that these species experience different selective pressures upon the timing of breeding, and hence responses to climate change may differ. Detailed information about life-history strategies is required to understand the effects of climate change, even in closely related taxa. The temporal match-mismatch hypothesis should be extended to consider subsequent critical periods when food needs to be abundantly available.

Transgenerational effects enhance specific immune response in a wild passerine.

Vertebrate mothers transfer diverse compounds to developing embryos that can affect their development and final phenotype (i.e., maternal effects). However, the way such effects modulate offspring phenotype, in particular their immunity, remains unclear. To test the impact of maternal effects on offspring development, we treated wild breeding house sparrows (Passer domesticus) in Sevilla, SE Spain with Newcastle disease virus (NDV) vaccine. Female parents were vaccinated when caring for first broods, eliciting a specific immune response to NDV. The immune response to the same vaccine, and to the PHA inflammatory test were measured in 11-day-old chicks from their following brood. Vaccinated chicks from vaccinated mothers developed a stronger specific response that was related to maternal NDV antibody concentration while rearing their chicks. The chicks' carotenoid concentration and total antioxidant capacity in blood were negatively related to NDV antibody concentration, whereas no relation with PHA response was found. Specific NDV antibodies could not be detected in 11-day-old control chicks from vaccinated mothers, implying that maternally transmitted antibodies are not directly involved but may promote offspring specific immunity through a priming effect, while other immunity components remain unaffected. Maternally transmitted antibodies in the house sparrow are short-lived, depend on maternal circulation levels and enhance pre-fledging chick specific immunity when exposed to the same pathogens as the mothers.

Effects of Agricultural Management Policies on the Exposure of Black-Winged Stilts (Himantopus himantopus) Chicks to Cholinesterase-Inhibiting Pesticides in Rice Fields.

Levels of exposure to pesticides in rice fields can be significant depending on the environmental policies practiced. The aim of European Union integrated management policy is to reduce pesticide use and impact on environment. Rice fields provide an alternative breeding habitat for many waterbirds that are exposed to the pesticides used and therefore can be valuable indicators of their risk for wildlife. To evaluate integrated management success we examined exposure of Black-winged Stilts (Himantopus himantopus) to cholinesterase-inhibiting pesticides in rice fields under different types of management by measuring plasma cholinesterase activity. Cholinesterase activity was lower in birds sampled in (a) 2008 after a period of intense pesticide application, than in (b) 2005-2007 and 2011 in rice fields subject to integrated management in Doñana (SW Spain) and (c) in control natural wetlands in Spain and Morocco. During 2009 and 2010, cholinesterase activity was lower in rice fields in Doñana than in rice fields in Larache and Sidi Allal Tazi (NW Morocco). Our results suggest that integrated management successfully reduced the exposure of Black-winged Stilts to pesticides in most of the years. Care should be taken to implement mosquito and pest crop controls on time and with environmentally friendly products in order to reduce its impact on wildlife.

Determinants and short-term physiological consequences of PHA immune response in lesser kestrel nestlings.

Individual immune responses are likely affected by genetic, physiological, and environmental determinants. We studied the determinants and short-term consequences of Phytohaemagglutinin (PHA) induced immune response, a commonly used immune challenge eliciting both innate and acquired immunity, on lesser kestrel (Falco naumanni) nestlings in semi-captivity conditions and with a homogeneous diet composition. We conducted a repeated measures analyses of a set of blood parameters (carotenoids, triglycerides, ß-hydroxybutyrate, cholesterol, uric acid, urea, total proteins, and total antioxidant capacity), metabolic (resting metabolic rate), genotypic (MHC class II B heterozygosity), and biometric (body mass) variables. PHA challenge did not affect the studied physiological parameters on a short-term basis (<12 hr), except plasma concentrations of triglycerides and carotenoids, which decreased and increased, respectively. Uric acid was the only physiological parameter correlated with the PHA induced immune response (skin swelling), but the change of body mass, cholesterol, total antioxidant capacity, and triglycerides between sessions (i.e., post-pre treatment) were also positively correlated to PHA response. No relationships were detected between MHC gene heterozygosity or resting metabolic rate and PHA response. Our results indicate that PHA response in lesser kestrel nestlings growing in optimal conditions does not imply a severe energetic cost 12 hr after challenge, but is condition-dependent as a rapid mobilization of carotenoids and decrease of triglycerides is elicited on a short-term basis.

Immune response to Newcastle disease virus vaccination in a wild passerine.

We studied the immune response of wild House Sparrows (Passer domesticus) experimentally challenged with different doses of inactivated Newcastle disease virus (NDV) vaccine. We evaluated within-individual cell-mediated and humoral responses in birds kept in outdoor aviaries, over a 6-wk period. Nonbreeding adult House Sparrows developed a significant humoral response to NDV experimental vaccination within 1 wk postchallenge, as measured by hemagglutination inhibition assay; values increased until week 4 and persisted until week 6. Differences among treatments appeared by week 1, with individuals challenged with the highest dose (0.2 mL) eliciting a higher humoral response than the rest (n = 18). By week 4, all individuals vaccinated displayed an increased humoral response, with individuals challenged with the highest dose remaining significantly above responses of individuals vaccinated with the middle dose (0.1 mL, n = 14), but not the lowest dose (0.05 mL, n = 15). The middle and lowest dose responded similarly and significantly different from controls (n = 23). Differences persisted through week 6 postchallenge. Cell-mediated responses were independent of the experimental treatment. All individuals experienced a rise in granulocyte concentration, whereas lymphocyte and monocyte concentrations decreased, most likely as a result of captivity. Adult wild House Sparrows immunochallenged with inactivated NDV vaccine developed a specific humoral response, highlighting the utility of this technique in immunologic and evolutionary ecology studies in wild birds.

Interpopulation variation in contour feather structure is environmentally determined in great tits.

BACKGROUND: The plumage of birds is important for flying, insulation and social communication. Contour feathers cover most of the avian body and among other functions they provide a critical insulation layer against heat loss. Feather structure and composition are known to vary among individuals, which in turn determines variation in the insulation properties of the feather. However, the extent and the proximate mechanisms underlying this variation remain unexplored. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed contour feather structure from two different great tit populations adapted to different winter regimes, one northern population in Oulu (Finland) and one southern population in Lund (Sweden). Great tits from the two populations differed significantly in feather structure. Birds from the northern population had a denser plumage but consisting of shorter feathers with a smaller proportion containing plumulaceous barbs, compared with conspecifics from the southern population. However, differences disappeared when birds originating from the two populations were raised and moulted in identical conditions in a common-garden experiment located in Oulu, under ad libitum nutritional conditions. All birds raised in the aviaries, including adult foster parents moulting in the same captive conditions, developed a similar feather structure. These feathers were different from that of wild birds in Oulu but similar to wild birds in Lund, the latter moulting in more benign conditions than those of Oulu. CONCLUSIONS/SIGNIFICANCE: Wild populations exposed to different conditions develop contour feather differences either due to plastic responses or constraints. Environmental conditions, such as nutrient availability during feather growth play a crucial role in determining such differences in plumage structure among populations.

A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group.

Quaternary climatic oscillations have been considered decisive in shaping much of the phylogeographic structure around the Mediterranean Basin. Within this paradigm, peripheral islands are usually considered as the endpoints of the colonization processes. Here, we use nuclear and mitochondrial markers to investigate the phylogeography of the blue tit complex (blue tit Cyanistes caeruleus, Canary blue tit C. teneriffae and azure tit C. cyanus), and assess the role of the Canary Islands for the geographic structuring of genetic variation. The Canary blue tit exhibits strong genetic differentiation within the Canary Islands and, in combination with other related continental species, provides an ideal model in which to examine recent differentiation within a closely related group of continental and oceanic island avian species. We analysed DNA sequences from 51 breeding populations and more than 400 individuals in the blue tit complex. Discrepancies in the nuclear and mitochondrial gene trees provided evidence of a complex evolutionary process around the Mediterranean Basin. Coalescent analyses revealed gene flow between C. caeruleus and C. teneriffae suggesting a dynamic process with multiple phases of colonization and geographic overlapping ranges. Microsatellite data indicated strong genetic differentiation among the Canary Islands and between the Canary archipelago and the close continental areas, indicating limited contemporary gene flow. Diversification of the blue tit complex is estimated to have started during the early Pliocene (≈ 5 Ma), coincident with the end of Messinian salinity crisis. Phylogenetic analyses indicated that the North African blue tit is derived from the Canary blue tits, a pattern is avian 'back colonization' that contrasts with more traditionally held views of islands being sinks rather than sources.

Predator proximity as a stressor in breeding flycatchers: mass loss, stress protein induction, and elevated provisioning.

We investigated the physiological and behavioral consequences for prey breeding at different distances from a nesting predator. In a natural setting, Pied Flycatchers (Ficedula hypoleuca) made territory location decisions relative to established Sparrowhawk (Accipiter nisus) nests. From female flycatchers attending nests at different distances from Sparrowhawk nests, we measured body mass, blood stress protein (HSP60 and HSP70), and plasma immunoglobulin levels at the beginning (initial) and end (final) of the flycatcher breeding cycle, and provisioning rates during the nestling phase. We found that individuals breeding in closer proximity to Sparrowhawk nests, under higher perceived predation risk, showed significantly lower body mass, higher stress protein and immunoglobulin levels, and higher nestling provisioning rates compared to those individuals breeding farther away. Across the range of distances investigated (30-610 m), final stress protein levels decreased linearly with distance, whereas the final measures of the other variables showed unimodal trends, increasing or decreasing until an intermediate distance (approximately 350 m) and reversing the direction of the trend. Within 300 m, however, all measures showed significant linear associations with distance from the Sparrowhawk nest. Body mass and stress protein associations with distance from Sparrowhawk nests were only present during late breeding, and not in early incubation. Spatial proximity to Sparrowhawk nests consistently explained significant variation in both physiological and behavioral measures, despite the multitude of potential sources of variation for these measures in a natural setting. This suggests that predictable spatial patterns in these measures in avian communities are determined by the sites of breeding predators. Habitat selection decisions of migrant prey that vary only slightly spatially have consequences even at the cellular level, which plausibly have impacts on individual survival. In addition, this study suggests that predation risk is an important factor affecting physiological condition of prey, including stress protein induction in terrestrial vertebrates.

Specific appetite for carotenoids in a colorful bird.

BACKGROUND: Since carotenoids have physiological functions necessary for maintaining health, individuals should be selected to actively seek and develop a specific appetite for these compounds. METHODOLOGY/PRINCIPAL FINDINGS: Great tits Parus major in a diet choice experiment, both in captivity and the field, preferred carotenoid-enriched diets to control diets. The food items did not differ in any other aspects measured besides carotenoid content. CONCLUSIONS/SIGNIFICANCE: Specific appetite for carotenoids is here demonstrated for the first time, placing these compounds on a par with essential nutrients as sodium or calcium.

Metabolic adjustments in breeding female kittiwakes (Rissa tridactyla) include changes in kidney metabolic intensity.

Black-legged kittiwakes (BLKIs) reduce self-maintenance cost through reductions in mass-specific basal metabolic rate (BMR), body mass and the size of visceral organs during the chick-rearing period. In the present study, we measured kidney in vitro oxygen consumption and plasma 3,3',5-triiodo-L: -thyronine (T3) levels of incubating and chick-rearing female BLKIs, to test whether the decrease in BMR is caused mainly by decreased metabolic intensity or simply by reductions in the size of organs with high metabolic intensity. Body mass and body condition were lower in chick-rearing birds compared with the incubating birds. In contrast to the previous findings, however, the kidney mass did not differ between the two breeding stages. Plasma T3 levels decreased substantially during the breeding season, indicating a reduction in BMR. Over the same period, kidney mass-specific oxygen consumption decreased (by 17.2%) from the incubating to the chick-rearing stage. Thus, the reduction in BMR found in breeding BLKIs seems partly explained by adjustments in metabolic intensity of visceral organs. Lowered metabolic intensity of visceral organs would permit increased allocation of energy to offspring at the expense of their own self-maintenance.

Local adaptation to winter conditions in a passerine spreading north: a common-garden approach.

Sedentary passerine birds living in temperate and boreal regions need a high metabolic capacity for thermogenesis to survive winter conditions. As a consequence of the increased thermogenic capacity, basal energetic demands rise at a time when resources and time to acquire them decrease. In a previous study, great tits (Parus major) from two localities in Fennoscandia with contrasting winter conditions differed in their metabolic response to ambient temperature. To investigate the physiological basis underlying interpopulation differences we performed a common-garden experiment to test whether these differences were genetically based. We found basal metabolic rate to be higher in birds originating from transferred eggs from the southern population compared to the ones from the northern population, contrary to the relationship among birds living in their region of origin. Despite previous evidence suggesting that gene flow prevents local adaptation at the northern range limits of a species expanding northward, we found that great tits differ in their reaction norm to winter conditions according to the population of origin.

Seasonality in daily body mass variation in a hoarding boreal passerine.

We studied the body mass variation from autumn to winter, in a free-living population of willow tits ( Parus montanus), a food-hoarding passerine living year-round in boreal forests. Our aim was to find out whether this population exhibits 'winter fattening' as part of the annual body mass cycle. 'True winter fattening' is considered to be a strategic response to winter conditions. The strategy includes an increase in both the morning mass and the daily mass increase, as winter approaches. A multivariate approach was used to find which predictors (year, date, age, sex, body size, temperature and snow depth) explained the mass variation in birds measured twice per day. Morning mass variation was explained by sex, age, wing length and snow depth. Independently, date explained morning mass variation only in adult males. None of the predictors explained the variation observed in daily mass increase in any age or sex class. Therefore, we failed to detect winter fattening in our study population of willow tits. Response to increasing night length is not due to higher absolute intake, but to higher energy acquisition rate and decreased night-time energy consumption. The results suggest that willow tits at high latitudes manage increasing energy demands on a short-term basis and respond flexibly to changing conditions by adjusting foraging efficiency and especially night-time energy expenditure.