Constitutive innate immune defenses in relation to urbanization and population density in an urban bird, the feral pigeon Columba livia domestica.

Urbanization processes modulate the immunological challenges faced by animals. Urban habitat transformations reshape pathogen diversity and abundance, while high population density-common in urban exploiter species-promotes disease transmission. Responses to urbanization may include adaptive adjustments of constitutive innate immune defenses (e.g. complement system and natural antibodies [NAbs]), which serve as first-line protection against infections. Here, we investigated associations of habitat urbanization and host population density with complement and NAbs in an urban bird, the feral pigeon Columba livia domestica. To do so, we employed the hemolysis-hemagglutination assay to analyze nearly 200 plasma samples collected across urbanization and pigeon population density gradients in five major cities in Poland. We found a negative association between urbanization score and hemagglutination (i.e. NAbs activity), but not hemolysis (i.e. complement activity), indicating either immunosuppression or adaptive downregulation of this immune defense in highly transformed urban landscape. Population density was not significantly related to either immune parameter, providing no evidence for density-dependent modulation of immune defenses. At the same time, there was a negative association of hemolysis with condition (scaled mass index), suggesting resource allocation trade-offs or contrasting effects of the urban environment on immune defenses and body condition. The results demonstrate that habitat structure can be an important factor shaping the immune defenses of the feral pigeon, although these associations were not mediated by variation in population density. Our study highlights the complexity of the links between immune defenses in wildlife and urbanization and reinforces the need for comprehensive ecoimmunological studies on urban animals.

Urbanization is associated with non-coding polymorphisms in candidate behavioural genes in the Eurasian coot.

Extensive transformation of natural land cover into urbanized areas enhances accumulation of phenotypic differences between animals from urban and nonurban populations, but there is little information on whether these changes, especially in terms of animal behaviour and circadian rhythm, have a genetic basis. The aim of this study was to investigate genetic background of behavioural differences between four pairs of urban and nonurban populations of a common waterbird, the Eurasian coot Fulica atra. For this purpose, we quantified polymorphisms in personality-related candidate genes, previously reported to be associated with avian circadian rhythms and behavioural traits that may be crucial for urban life. We found general associations between landscape urbanization level and polymorphisms in 3'UTR region of CREB1 gene encoding transcriptional factor, which participates in development of cognitive functions and regulation of circadian rhythm. We also found significant differentiation between urban and nonurban populations in the intronic region of CKIɛ gene responsible for regulation of circadian clock. Although we lacked evidence for linkage of this intronic variation with coding polymorphisms, genetic differentiation between urban populations was significantly stronger at CKIɛ intron compared with neutral microsatellite markers, suggesting possible local adaptations of CKIɛ expression regulation to specific urban sites. Our results indicate that behavioural differentiation between urban and nonurban coot populations may be the effect of habitat-specific selective pressure resulting in genetic adaptations to urban environment and supporting the microevolutionary scenario. These adaptations, however, prevailed in non-coding regulatory rather than coding gene regions and showed either general or local patterns, revealing high complexity of associations between behaviour and landscape urbanization in birds.

Genetic variation at innate and adaptive immune genes - contrasting patterns of differentiation and local adaptation in a wild gull.

Immunogenetic variation in natural vertebrate populations is expected to respond to spatial and temporal fluctuations in pathogen assemblages. While spatial heterogeneity in pathogen-driven selection enhances local immunogenetic adaptations and population divergence, different immune genes may yield contrasting responses to the environment. Here, we investigated population differentiation at the key pathogen recognition genes of the innate and adaptive immune system in a colonial bird species, the black-headed gull Chroicocephalus ridibundus. We assessed genetic variation at three toll-like receptor (TLR) genes (innate immunity) and the major histocompatibility complex (MHC) class I and II genes (adaptive immunity) in gulls from seven colonies scattered across Poland. As expected, we found much greater polymorphism at the MHC than TLRs. Population differentiation at the MHC class II, but not MHC-I, was significantly stronger than at neutral microsatellite loci, suggesting local adaptation. This could reflect spatial variation in the composition of extracellular parasite communities (e.g., helminths), possibly driven by sharp differences in habitat structure between colonies. Despite contrasting patterns of population differentiation, both MHC classes showed similar regimes of diversifying selection. Some significant population differentiation was also observed at TLRs, suggesting that innate immune receptors may respond to fine-scale spatial variation in pathogen pressure, although this pattern could have been enhanced by drift. Our results suggested that local adaptation at the pathogen recognition immune genes can be maintained at relatively small or moderate spatial scales in species with high dispersal potential and they highlighted the complexity of immunogenetic responses of animals to heterogeneous environments.

Contrasting haemoparasite prevalence in larid species with divergent ecological niches and migration patterns.

Haemoparasites represent a diverse group of vector-borne parasites that infect a wide range of vertebrate hosts. In birds, haemoparasite infection rates may be associated with various ecological and life history traits, including habitat choice, colony size and migration distance. Here, we molecularly assessed the prevalence of 3 main haemoparasite genera (Plasmodium, Haemoproteus and Leucocytozoon) in 2 bird species with different habitat preferences and migratory behaviour: black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo). We found that gulls showed a much higher prevalence and diversity of Plasmodium or Haemoproteus (ca. 60% of individuals infected) than terns (zero prevalence). The prevalence of Leucocytozoon was low in both species (<3%). The differences in haemoparasite prevalences may be primarily driven by varying vector encounter rate resulting from different habitat preferences, as black-headed gulls mainly use vector-rich vegetated freshwater habitats, whereas common terns often use vector-poor coastal and brackish habitats. Since common terns migrate further than black-headed gulls, our results did not provide support for an association between haemoparasite prevalence and migratory distance. In gulls, we found a negative association between colony size and infection rates, suggestive of an ideal despotic distribution, and phylogenetic analyses of detected haemoparasite lineages provided evidence for higher host specificity in Haemoproteus than Plasmodium. Our results suggest that the preference for coastal areas and less vegetated habitats in terns may reduce haemoparasite infection rates compared to other larids, regardless of their migratory distance, emphasizing the role of ecological niches in parasite exposure.

Population density mediates induced immune response, but not physiological condition in a well-adapted urban bird.

Thriving under high population density is considered a major feature of urban exploiter species. Nevertheless, population density appears to be a surprisingly overlooked factor in urban ecology studies. High population numbers observed in urban species might promote pathogen transmission and negatively affect health or condition, thus requiring investments in immunocompetence. The feral pigeon Columba livia domestica is an example of a successful city-dweller, found in great abundance in large cities across the globe. We investigated the effects of population density on induced immune response (phytohaemagglutinin skin test) and body condition (blood haemoglobin concentration and size-corrected body mass) in 120 feral pigeons, captured along population density gradient in Lódz (central Poland). We found that stronger immune response was associated with higher population density, but was not related to physiological condition and physiological stress (heterophil/lymphocyte ratio). Moreover, condition indices were not associated with population density. However, since pigeon population density was highly correlated with the level of habitat urbanization, we cannot exclude that any density-dependent effects may be mediated by habitat variation. Our results indicate that urban environment, via population density, might exert different selective pressures on immunocompetence and body condition in this successful urban exploiter.

Complex associations of weather conditions with reproductive performance in urban population of a common waterbird.

Weather conditions are recognized as one of key determinants of animal reproductive performance; however, the effect of weather on breeding success can be modulated by different features of breeding habitat. Constantly expanding urban areas cause significant changes in land cover and environmental conditions, but whether and how urban landscape mitigates weather impact on animal fitness remains little explored. The aim of this study was to investigate the association between weather parameters and reproductive performance in a reed-nesting waterbird species, the Eurasian coot Fulica atra. For this purpose, we performed a long-term monitoring of an urban coot population from central Poland, collecting data for over 400 breeding events. The results indicated that temperature may have contrasting effects on coot reproductive output at different stages of chick-rearing period (positive at early chick-rearing and negative at late chick-rearing). Also, contrary to our expectation, we found a positive relationship between mean daily precipitation in early chick-rearing period and reproductive output in our study population. Our study constitutes one of few examples showing how weather may affect fitness in urban wildlife and provides evidence for high complexity of associations between weather conditions and animal reproductive performance.

Consistent choice of landscape urbanization level across the annual cycle in a migratory waterbird species.

Rapid urbanization has a great impact on avian distribution, ecology, habitat selection, and behavior. Recent avian studies indicated that individuals remain consistent in their behavioral responses to human disturbance across short periods of time. However, there is still little information about keeping consistent behaviors in distinct locations across different stages of the annual cycle. In this study, we aimed to test for long-term consistency in habitat selection with respect to urbanization in a migratory waterbird species, the Eurasian coot Fulica atra. For this purpose, we individually marked ca. 300 coots from four populations that varied in urbanization level and tracked their habitat preferences during the non-breeding season. We found that individuals from urban breeding populations selected habitats with a higher share of artificial areas during the non-breeding season, when compared to non-urban individuals. Also, a comparison of non-breeding sites selected by birds from our study populations with random sites showed that urban birds selected sites with higher urbanization level than resulting from random availability. Finally, we found a seasonal variation in habitat preferences in coots-individuals from all study populations selected more urbanized areas as the non-breeding season progressed. The results indicate that birds are able to remain consistent in habitat preferences not only at a large geographical scale, but also across different seasons. Marked between-population variation in habitat selection across the annual cycle may reflect personality differences of coots from urban and non-urban populations, and it stays in line with the personality-matching habitat choice hypothesis.