Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

Adaptive phenotypic and genomic divergence in the common chaffinch (Fringilla coelebs) following niche expansion within a small oceanic island.

According to models of ecological speciation, adaptation to adjacent, contrasting habitat types can lead to population divergence given strong enough environment-driven selection to counteract the homogenizing effect of gene flow. We tested this hypothesis in the common chaffinch (Fringilla coelebs) on the small island of La Palma, Canary Islands, where it occupies two markedly different habitats. Isotopic (δ13 C, δ15 N) analysis of feathers indicated that birds in the two habitats differed in ecosystem and/or diet, and analysis of phenotypic traits revealed significant differences in morphology and plumage colouration that are consistent with ecomorphological and ecogeographical predictions respectively. A genome-wide survey of single-nucleotide polymorphism revealed marked neutral structure that was consistent with geography and isolation by distance, suggesting low dispersal. In contrast, loci putatively under selection identified through genome-wide association and genotype-environment association analyses, revealed amarked adaptive divergence between birds in both habitats. Loci associated with phenotypic and environmental differences among habitats were distributed across the genome, as expected for polygenic traits involved in local adaptation. Our results suggest a strong role for habitat-driven local adaptation in population divergence in the chaffinches of La Palma, a process that appears to be facilitated by a strong reduction in effective dispersal distances despite the birds' high dispersal capacity.

Integrating population connectivity into pollution assessment: Overwintering mixing reveals flame retardant contamination in breeding areas in a migratory raptor.

Determining the exposure and magnitude at which various pollutants are differentially assimilated at the breeding and non-breeding grounds of migratory wildlife is challenging. Here, the possibility of applying the migratory connectivity framework to understanding contamination in birds is illustrated by considering flame retardants in inviable eggs of a migratory raptor, the black kite (Milvus migrans). The occurrence and concentration of legacy and emerging compounds in eggs from the southeastern peri-urban area of Madrid city, central Spain, were compared with those from Doñana National Park in southern Spain. A much higher occurrence and concentration of multiple polybrominated diphenyl ethers and Dechlorane 602 were found in Madrid than Doñana, but the opposite patterns were found for Dechlorane Plus. Individuals from these and other breeding areas in western Europe showed a strong intermixing pattern over widespread wintering areas in Africa, as assessed by ringing recoveries and movements tracked by satellite devices. This diffuse migratory connectivity reveals breeding areas as the main contamination grounds. High contamination burdens sequestered in eggs point to rapid assimilation of these compounds before laying, associated with important emission sources in Madrid, especially landfills of partially incinerated urban refuse, and other anthropogenic operations. Diet composition regarding aquatic vs. terrestrial prey, and bioaccumulation and biomagnification processes are suggested to explain differential assimilation of some compounds, especially Dechlorane Plus in Doñana, although a local emission source polluting this area cannot be ruled out. Insight from the migratory connectivity framework can help to disentangle large-scale patterns of contaminant uptake and refocus attention on key regions and potential causes of chemical hazards in declining migratory species and human populations.

Extreme genetic structure in a social bird species despite high dispersal capacity.

Social barriers have been shown to reduce gene flow and contribute to genetic structure among populations in species with high cognitive capacity and complex societies, such as cetaceans, apes and humans. In birds, high dispersal capacity is thought to prevent population divergence unless major geographical or habitat barriers induce isolation patterns by dispersal, colonization or adaptation limitation. We report that Iberian populations of the red-billed chough, a social, gregarious corvid with high dispersal capacity, show a striking degree of genetic structure composed of at least 15 distinct genetic units. Monitoring of marked individuals over 30 years revealed that long-distance movements over hundreds of kilometres are common, yet recruitment into breeding populations is infrequent and highly philopatric. Genetic differentiation is weakly related to geographical distance, and habitat types used are overall qualitatively similar among regions and regularly shared by individuals of different populations, so that genetic structure is unlikely to be due solely to isolation by distance or isolation by adaptation. Moreover, most population nuclei showed relatively high levels of genetic diversity, suggesting a limited role for genetic drift in significantly differentiating populations. We propose that social mechanisms may underlie this unprecedented level of genetic structure in birds through a pattern of isolation by social barriers not yet described, which may have driven this remarkable population divergence in the absence of geographical and environmental barriers.

Oral disease is linked to low nestling condition and brood size in a raptor species living in a highly modified environment.

Anthropogenic stressors can favor the occurrence of noninfectious disease that can be worsened by the impact of opportunistic pathogens, making the epizootiology of environmental diseases difficult to unravel. The incidence and impact of oral lesions in nestlings of a facultative scavenger species, the black kite Milvus migrans, were examined over seven breeding seasons in the highly degraded environment close to Madrid, Spain. We found an overall prevalence of 31% of nestlings with oral lesions, with no clear spatial pattern in nests with affected and unaffected individuals. The occurrence and number of oral lesions were negatively associated with nestling body condition and brood size. Broods, where all siblings had oral lesions, were smaller than those where some or all siblings were apparently healthy, suggesting that oral disease could be causing nestling mortality and, consequently, brood size reduction. In turn, nestling body condition was negatively affected by lesion occurrence, brood size, and laying date. Although these relationships were bidirectional, piecewise structural equation modeling analyses showed a greater negative effect of body condition on lesion occurrence than vice versa, indicating that nestlings in poorer body condition were more likely to develop oral lesions (which could contribute to aggravate their state of deterioration) than those in better condition. Nestlings from small broods were also more likely to have oral disease (directly or indirectly through their lower body condition) than nestlings from large broods. Nestlings that hatched last in the broods showed greater development stress than those that hatched first. Anthropogenic stressors could trigger poor body condition, and contribute to microbiota dysbiosis-related diseases. Although further research is needed to determine the consequences for the long-term fitness of individuals, actions should be taken to mitigate adverse conditions that may favor the appearance of environmental diseases associated with peri-urban areas, given their rapid expansion over natural areas.

Domestic Waste and Wastewaters as Potential Sources of Pharmaceuticals in Nestling White Storks (Ciconia ciconia).

Information on the exposure of wild birds to pharmaceuticals from wastewater and urban refuse is scarce despite the enormous amount of drugs consumed and discarded by human populations. We tested for the presence of a battery of antibiotics, NSAIDs, and analgesics in the blood of white stork (Ciconia ciconia) nestlings in the vicinity of urban waste dumps and contaminated rivers in Madrid, central Spain. We also carried out a literature review on the occurrence and concentration of the tested compounds in other wild bird species to further evaluate possible shared exposure routes with white storks. The presence of two pharmaceutical drugs (the analgesic acetaminophen and the antibiotic marbofloxacin) out of fourteen analysed in the blood of nestlings was confirmed in 15% of individuals (n = 20) and in 30% of the nests (n = 10). The apparently low occurrence and concentration (acetaminophen: 9.45 ng mL-1; marbofloxacin: 7.21 ng mL-1) in nestlings from different nests suggests the uptake through food acquired in rubbish dumps rather than through contaminated flowing water provided by parents to offspring. As with other synthetic materials, different administration forms (tablets, capsules, and gels) of acetaminophen discarded in household waste could be accidentally ingested when parent storks forage on rubbish to provide meat scraps to their nestlings. The presence of the fluoroquinolone marbofloxacin, exclusively used in veterinary medicine, suggests exposure via consumption of meat residues of treated animals for human consumption found in rubbish dumps, as documented previously at higher concentrations in vultures consuming entire carcasses of large livestock. Control measures and ecopharmacovigilance frameworks are needed to minimize the release of pharmaceutical compounds from the human population into the environment.

Insularity determines nestling sex ratio variation in Egyptian vulture populations.

Variation in offspring sex ratio, particularly in birds, has been frequently studied over the last century, although seldom using long-term monitoring data. In raptors, the cost of raising males and females is not equal, and several variables have been found to have significant effects on sex ratio, including food availability, parental age, and hatching order. Sex ratio differences between island populations and their mainland counterparts have been poorly documented, despite broad scientific literature on the island syndrome reporting substantial differences in population demography and ecology. Here, we assessed individual and environmental factors potentially affecting the secondary sex ratio of the long-lived Egyptian vulture Neophron percnopterus. We used data collected from Spanish mainland and island populations over a ca. 30-year period (1995-2021) to assess the effects of insularity, parental age, breeding phenology, brood size, hatching order, type of breeding unit (pairs vs. trios), and spatial and temporal variability on offspring sex ratio. No sex bias was found at the population level, but two opposite trends were observed between mainland and island populations consistent with the island syndrome. Offspring sex ratio was nonsignificantly female-biased in mainland Spain (0.47, n = 1112) but significantly male-biased in the Canary Islands (0.55, n = 499), where a male-biased mortality among immatures could be compensating for offspring biases and maintaining a paired adult sex ratio. Temporal and spatial variation in food availability might also have some influence on sex ratio, although the difficulties in quantifying them preclude us from determining the magnitude of such influence. This study shows that insularity influences the offspring sex ratio of the Egyptian vulture through several processes that can affect island and mainland populations differentially. Our research contributes to improving our understanding of sex allocation theory by investigating whether sex ratio deviations from parity are possible as a response to changing environments comprised by multiple and complexly interrelated factors.

Phenotypic and environmental correlates of natal dispersal in a long-lived territorial vulture.

Natal dispersal, the movement between the birth and the first breeding site, has been rarely studied in long-lived territorial birds with a long-lasting pre-breeding stage. Here we benefited from the long-term monitoring programs of six populations of Egyptian vultures (Neophron percnopterus) from Spain and France to study how the rearing environment determines dispersal. For 124 vultures, we recorded a median dispersal distance of 48 km (range 0-656 km). Linear models were used to assess the effect of population and individual traits on dispersal distance at two spatial scales. Dispersal distances were inversely related to vulture density in the natal population, suggesting that birds perceive the abundance of conspecifics as a signal of habitat quality. This was particularly true for declining populations, so increasing levels of opportunistic philopatry seemed to arise in high density contexts as a consequence of vacancies created by human-induced adult mortality. Females dispersed further than males, but males were more sensitive to the social environment, indicating different dispersal tactics. Both sexes were affected by different individual attributes simultaneously and interactively with this social context. These results highlight that complex phenotype-by-environment interactions should be considered for advancing our understanding of dispersal dynamics in long-lived organisms.

Influence of habitat suitability and sex-related detectability on density and population size estimates of habitat-specialist warblers.

Knowledge about the population size and trends of common bird species is crucial for setting conservation priorities and management actions. Multi-species large-scale monitoring schemes have often provided such estimates relying on extrapolation of relative abundances in particular habitats to large-scale areas. Here we show an alternative to inference-rich predictive models, proposing methods to deal with caveats of population size estimations in habitat-specialist species, reed warblers (Acrocephalus scirpaceus and Acrocephalus arundinaceus). Reed warblers were only found in pure reedbeds within riparian woodlands or in riparian vegetation scattered within or around reedbed patches, as expected according to their habitat specialization. The proportion of individuals located in reedbed associated with lotic and lentic waters differed between species, and no reed warbler was recorded in reedbed located along dry streams. This indicates that microhabitat features or their effects on reedbed structure and other factors made a proportion of the apparently available habitat unsuitable for both warbler species. Most warblers detected were males performing territorial singing (females seldom sing and do not perform elaborate territorial song, and are undistinguishable from males by plumage). The regional population sizes of the warbler species (~4000 individuals of A. scirpaceus and ~ 1000 individuals of A. arundinaceus) were much smaller than those estimated for the same area by transforming relative abundance obtained at a national scale to population size through extrapolation by habitat at a regional scale. These results highlight the importance of considering the habitat actually used and its suitability, the manner of sex-related detection, population sex-ratio and their interactions in population estimates. Ideally, the value of predictive methods to estimate population size of common species should be tested before conducting large-scale monitoring, rather than a posteriori. Although logistically challenging, this can be achieved by designing monitoring programs including an intensive sampling of abundance in ad hoc reference areas of variable size.

Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feather carotenoproteins?

Several avian species show a bright carotenoid-based coloration during spring and following a period of duller coloration during the previous winter, despite carotenoids presumably being fully deposited in feathers during the autumn moult. Carotenoid-based breast feathers of male linnets (Carduelis cannabina) increased in hue (redness), saturation and brightness after exposing them to outdoor conditions from winter to spring. This represents the first experimental evidence showing that carotenoid-based plumage coloration may increase towards a colourful expression due to biotic or abiotic environmental factors acting directly on full-grown feathers when carotenoids may be fully functional. Sunlight ultraviolet (UV) irradiation was hypothesized to denature keratin and other proteins that might protect pigments from degradation by this and other environmental factors, suggesting that sunlight UV irradiation is a major factor in the colour increase from winter to spring. Feather proteins and other binding molecules, if existing in the follicles, may be linked to carotenoids since their deposition into feathers to protect colourful features of associated carotenoids during the non-breeding season when its main signalling function may be relaxed. Progress towards uncovering the significance of concealment and subsequent display of colour expression should consider the potential binding and protecting nature of feather proteins associated with carotenoids.

Age-Related Relationships between Innate Immunity and Plasma Carotenoids in an Obligate Avian Scavenger.

Variation in immunity is influenced by allocation trade-offs that are expected to change between age-classes as a result of the different environmental and physiological conditions that individuals encounter over their lifetime. One such trade-off occurs with carotenoids, which must be acquired with food and are involved in a variety of physiological functions. Nonetheless, relationships between immunity and carotenoids in species where these micronutrients are scarce due to diet are poorly studied. Among birds, vultures show the lowest concentrations of plasma carotenoids due to a diet based on carrion. Here, we investigated variations in the relationships between innate immunity (hemagglutination by natural antibodies and hemolysis by complement proteins), pathogen infection and plasma carotenoids in nestling and adult griffon vultures (Gyps fulvus) in the wild. Nestlings showed lower hemolysis, higher total carotenoid concentration and higher pathogen infection than adults. Hemolysis was negatively related to carotenoid concentration only in nestlings. A differential carotenoid allocation to immunity due to the incomplete development of the immune system of nestlings compared with adults is suggested linked to, or regardless of, potential differences in parasite infection, which requires experimental testing. We also found that individuals with more severe pathogen infections showed lower hemagglutination than those with a lower intensity infection irrespective of their age and carotenoid level. These results are consistent with the idea that intraspecific relationships between innate immunity and carotenoids may change across ontogeny, even in species lacking carotenoid-based coloration. Thus, even low concentrations of plasma carotenoids due to a scavenger diet can be essential to the development and activation of the immune system in growing birds.

Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca.

We report a field study of the haematocrit of pied flycatcher (Ficedula hypoleuca) nestlings when close to fledging. First a descriptive study was conducted of both fledgling and adult haematocrit over 2 years to analyse correlates of variation in this trait. Then a swapping experiment was performed to see whether variation among fledglings had a measurable genetic component. Average fledgling haematocrits were lower than those of their male and female parents. Intraclass correlations among sibships in fledgling haematocrit were high in both years, indicating that the estimates of resemblance were inflated, probably by common environmental effects. Fledgling haematocrits were unrelated to date and number of young in the nest. Fledglings with a high haematocrit were heavy and had thick breast muscles. There were no significant relationships between the average fledgling haematocrit and those of the adults caring for them. Nest mite ectoparasites negatively affected fledgling haematocrit. The haematocrits of adults did not differ between sexes or years and in both sexes were unrelated to breeding date, body mass, age, clutch size or number of young reared. Females, but not males, caring for fledglings in nests infested by mites had a lower haematocrit than those rearing young in mite-free nests. The cross-fostering experiment indicated that almost all measured variation in haematocrit was explained by the nest where the bird was reared (67.2% of the explained variance), not by their nest of origin (7.8%), meaning that there was a very small, non-significant resemblance in the haematocrit of genetically related sibs when reared in different environments while unrelated nestlings reared in the same nestbox had similar haematocrits. The low proportion of variance explained by the familial component may be due to the high connection of haematocrit to fitness.

Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid-waste incinerator.

Exposure to heavy metals from emissions of the solid-waste incinerator (SWI) of Madrid (Spain) was assessed by determining the relationships between the distance from black kite (Milvus migrans) nests to the SWI and metal concentrations in nestling blood and failed eggs. Lead levels increased as the distance to the SWI decreased, while no significant relationship was found for the remaining elements. Analysis of frequency distributions showed that Pb was normally distributed, suggesting a generalized exposure to this contaminant. Variability in metal levels within and between nests indicated a differential nest exposure to contaminant metals with sibling chicks showing similar metal levels. Correlations between essential and contaminant metals suggested detoxifying mechanisms mediated by essential metals. The contribution of metal residues in blood coming from deposition in eggs was minimal compared with residues coming from posthatch exposure. Exposure to particulate volatile Pb in the form of dust from fly ash emitted to the air by the SWI is suggested to be the main route of uptake via inhalation, while both dietary and respiratory routes may contribute to Cd uptake. The increasing human population living close to the SWI may be increasingly at risk from exposure to air-borne contaminants depending on the emission standards from the SWI.

Repeatability of feather mite prevalence and intensity in passerine birds.

Understanding why host species differ so much in symbiont loads and how this depends on ecological host and symbiont traits is a major issue in the ecology of symbiosis. A first step in this inquiry is to know whether observed differences among host species are species-specific traits or more related with host-symbiont environmental conditions. Here we analysed the repeatability (R) of the intensity and the prevalence of feather mites to partition within- and among-host species variance components. We compiled the largest dataset so far available: 119 Paleartic passerine bird species, 75,944 individual birds, ca. 1.8 million mites, seven countries, 23 study years. Several analyses and approaches were made to estimate R and adjusted repeatability (R(adj)) after controlling for potential confounding factors (breeding period, weather, habitat, spatial autocorrelation and researcher identity). The prevalence of feather mites was moderately repeatable (R = 0.26-0.53; R(adj) = 0.32-0.57); smaller values were found for intensity (R = 0.19-0.30; R(adj )= 0.18-0.30). These moderate repeatabilities show that prevalence and intensity of feather mites differ among species, but also that the high variation within species leads to considerable overlap among bird species. Differences in the prevalence and intensity of feather mites within bird species were small among habitats, suggesting that local factors are playing a secondary role. However, effects of local climatic conditions were partially observed for intensity.

Geographical variation in cloacal microflora and bacterial antibiotic resistance in a threatened avian scavenger in relation to diet and livestock farming practices.

The impact on wildlife health of the increase in the use of antimicrobial agents with the intensification of livestock production remains unknown. The composition, richness and prevalence of cloacal microflora as well as bacterial resistance to antibiotics in nestlings and full-grown Egyptian vultures Neophron percnopterus were assessed in four areas of Spain in which the degree of farming intensification differs. Differences in diet composition, especially the role of stabled livestock carrion, appear to govern the similarities of bacterial flora composition among continental populations, while the insular vulture population (Fuerteventura, Canary Islands) showed differences attributed to isolation. Evidence of a positive relationship between the consumption of stabled livestock carrion and bacterial resistance to multiple antibiotics was found. Bacterial resistance was high for semisynthetic penicillins and enrofloxacin, especially in the area with the most intensive stabled livestock production. The pattern of antibiotic resistance was similar for the different bacterial species within each area. Bacterial resistance to antibiotics may be determined by resistance of bacteria present in the livestock meat remains that constituted the food of this species, as indicated by the fact that resistance to each antibiotic was correlated in Escherichia coli isolated from swine carrion and Egyptian vulture nestlings. In addition, resistance in normal faecal bacteria (present in the microflora of both livestock and vultures) was higher than in Staphylococcus epidermidis, a species indicator of the transient flora acquired presumably through the consumption of wild rabbits. Potential negative effects of the use of antimicrobials in livestock farming included the direct ingestion of these drug residues and the effects of bacterial antibiotic resistance on the health of scavengers.

Contamination with nonessential metals from a solid-waste incinerator correlates with nutritional and immunological stress in prefledgling black kites (Milvus migrans).

We assessed whether levels of heavy metals in blood have detrimental effects on the health of prefledgling black kites (Milvus migrans) exposed to emissions from a solid waste incinerator near Madrid, central Spain. As health indexes, we considered body mass corrected by structural size as a general indicator of nutritional condition and white blood cell counts (especially the heterophil:lymphocyte ratio) as an indirect measure of immune function. Nutritional condition was positively related to levels of Zn, an essential element with a major role in many physiological pathways, while the opposite trend was found for the essential Cu, the concentration of which tends to increase with decreasing nutritional condition. We found an interaction between Zn and Cd, indicating that high levels of Zn produce smaller effects of Cd on body mass. Potential immunological stress, expressed as an increase in the heterophil:lymphocyte ratio, caused by the toxic Cd increased as levels of Cu decreased. Thus, nestlings with low levels of Cu and poor nutritional condition suffered more immunological stress due to Cd contamination than nestlings with higher levels of Cu. We also found a negative interaction between Zn and Cd, indicating a response of essential Zn to increasing levels of Cd, which may be indicative of the negative effects of Cd on the immune system. These results suggest that the participation of metallothioneins in detoxification and metal regulation may also indirectly enhance the adrenal stress response to contaminants, probably through a competition of Cd and Zn for Zn binding sites on metallothioneins, reducing the ability of Cd to stress the immune system.