Roberto Ambrosini

Climate warming, ecological mismatch at arrival and population decline in migratory birds

Climate is changing at a fast pace, causing widespread, profound consequences for living organisms. Failure to adjust the timing of life-cycle events to climate may jeopardize populations by causing ecological mismatches to the life cycle of other species and abiotic factors. Population declines of some migratory birds breeding in Europe have been suggested to depend on their inability to adjust migration phenology so as to keep track of advancement of spring events at their breeding grounds. In fact, several migrants have advanced their spring arrival date, but whether such advancement has been sufficient to compensate for temporal shift in spring phenophases or, conversely, birds have become ecologically mismatched, is still an unanswered question, with very few exceptions. We used a novel approach based on accumulated winter and spring temperatures (degree-days) as a proxy for timing of spring biological events to test if the progress of spring at arrival to the breeding areas by 117 European migratory bird species has changed over the past five decades. Migrants, and particularly those wintering in sub-Saharan Africa, now arrive at higher degree-days and may have therefore accumulated a ‘thermal delay’, thus possibly becoming increasingly mismatched to spring phenology. Species with greater ‘thermal delay’ have shown larger population decline, and this evidence was not confounded by concomitant ecological factors or by phylogenetic effects. These findings provide general support to the largely untested hypotheses that migratory birds are becoming ecologically mismatched and that failure to respond to climate change can have severe negative impacts on their populations. The novel approach we adopted can be extended to the analysis of ecological consequences of phenological response to climate change by other taxa.

Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of Northern Italy

Despite airborne microorganisms representing a relevant fraction of atmospheric suspended particles, only a small amount of information is currently available on their abundance and diversity and very few studies have investigated the environmental factors influencing the structure of airborne bacterial communities. In this work, we used quantitative PCR and Illumina technology to provide a thorough description of airborne bacterial communities in the urban area of Milan (Italy). Forty samples were collected in 10-day sampling sessions, with one session per season. The mean bacterial abundance was about 104 ribosomal operons per m3 of air and was lower in winter than in the other seasons. Communities were dominated by Actinobacteridae, Clostridiales, Sphingobacteriales and few proteobacterial orders (Burkholderiales, Rhizobiales, Sphingomonadales and Pseudomonadales). Chloroplasts were abundant in all samples. A higher abundance of Actinobacteridae, which are typical soil-inhabiting bacteria, and a lower abundance of chloroplasts in samples collected on cold days were observed. The variation in community composition observed within seasons was comparable to that observed between seasons, thus suggesting that airborne bacterial communities show large temporal variability, even between consecutive days. The structure of airborne bacterial communities therefore suggests that soil and plants are the sources which contribute most to the airborne communities of Milan atmosphere, but the structure of the bacterial community seems to depend mainly on the source of bacteria that predominates in a given period of time.

Unravelling the bacterial diversity in the atmosphere.

The study of airborne biological particles (‘bioaerosols’) has gained interest in recent years, due to an increasing amount of evidence suggesting that this fraction of airborne particulate matter may play a critical role in the negative effects of aerosols on biological systems. Pioneer investigations demonstrated that bacteria do exist in the atmosphere and can be metabolically active, although studies have not proved whether they actually form ecological communities or are merely assemblages of organisms passively transported from different sources. For a long time, cultivation-based methods have been the gold standard to describe and quantify airborne microorganisms. However, the use of culture-independent techniques and, more recently, of the next-generation sequencing-based methods, has improved the ability of the scientific community to investigate bioaerosols in detail and to address further research questions, such as the temporal and spatial variability of airborne bacterial assemblages, the environmental factors affecting this variability and the potential sources of atmospheric bacteria. This paper provides a systematic review of the state-of-the-art methodologies used in the study of airborne bacteria to achieve each of the aforementioned research objectives, as well as the main results obtained so far. Critical evaluations of the current state of the knowledge and suggestions for further researches are provided.

Sexual Dimorphism in Melanin Pigmentation, Feather Coloration and Its Heritability in the Barn Swallow (Hirundo rustica)

Melanin is the main pigment in animal coloration and considerable variation in the concentrations of the two melanin forms (pheo- and eumlanin) in pigmented tissues exists among populations and individuals. Melanin-based coloration is receiving increasing attention particularly in socio-sexual communication contexts because the melanocortin system has been hypothesized to provide a mechanistic basis for covariation between coloration and fitness traits. However, with few notable exceptions, little detailed information is available on inter-individual and inter-population variation in melanin pigmentation and on its environmental, genetic and ontogenetic components. Here, we investigate melanin-based coloration in an Italian population of a passerine bird, the barn swallow (Hirundo rustica rustica), its sex- and age-related variation, and heritability. The concentrations of eu- and pheomelanin in the throat (brown) and belly (white-to-brownish) feathers differed between sexes but not according to age. The relative concentration of either melanin (Pheo:Eu) differed between sexes in throat but not in belly feathers, and the concentrations in males compared to females were larger in belly than in throat feathers. There were weak correlations between the concentrations of melanins within as well as among plumage regions. Coloration of belly feathers was predicted by the concentration of both melanins whereas coloration of throat feathers was only predicted by pheomelanin in females. In addition, Pheo:Eu predicted coloration of throat feathers in females and that of belly feathers in males. Finally, we found high heritability of color of throat feathers. Melanization was found to differ from that recorded in Hirundo rustica rustica from Scotland or from H. r. erythrogaster from North America. Hence, present results show that pigmentation strategies vary in a complex manner according to sex and plumage region, and also among geographical populations, potentially reflecting adaptation to different natural and sexual selection regimes, and that some coloration components seem to be highly heritable.

Viability Is Associated with Melanin-Based Coloration in the Barn Swallow (Hirundo rustica)

Pigmentation of body surface in animals can have multiple determinants and accomplish diverse functions. Eumelanin and pheomelanin are the main animal pigments, being responsible of yellow, brownish-red and black hues, and have partly common biosynthetic pathways. Many populations of vertebrates show individual variation in melanism, putatively with large heritable component. Genes responsible for eu- or pheomelanogenesis have pleiotropic but contrasting effects on life-history traits, explaining the patterns of covariation observed between melanization and physiology (e.g. immunity and stress response), sexual behavior and other characters in diverse taxa. Yet, very few studies in the wild have investigated if eu- and pheomelanization predict major fitness traits like viability or fecundity. In this correlative study, by contrasting adult barn swallows (Hirundo rustica) matched for age, sex, breeding site, and year and date of sampling, we show that males but not females that survived until the next year had paler, relatively more eu- than pheomelanic pigmentation of ventral body feathers. Better performance of individuals that allocate relatively more to eumelanogenesis was expected based on previous evidence on covariation between eumelanic pigmentation and specific traits related to immunity and susceptibility to stress. However, together with the evidence of no covariation between viability and melanization among females, this finding raises the question of the mechanisms that maintain variation in genes for melanogenesis. We discuss the possibility that eu- and pheomelanization are under contrasting viability and sexual selection, as suggested by larger breeding and sperm competition success of darker males from other barn swallow subspecies.

Spatio-temporal variability of airborne bacterial communities and their correlation with particulate matter chemical composition across two urban areas

The study of spatio-temporal variability of airborne bacterial communities has recently gained importance due to the evidence that airborne bacteria are involved in atmospheric processes and can affect human health. In this work, we described the structure of airborne microbial communities in two urban areas (Milan and Venice, Northern Italy) through the sequencing, by the Illumina platform, of libraries containing the V5–V6 hypervariable regions of the 16S rRNA gene and estimated the abundance of airborne bacteria with quantitative PCR (qPCR). Airborne microbial communities were dominated by few taxa, particularly Burkholderiales and Actinomycetales, more abundant in colder seasons, and Chloroplasts, more abundant in warmer seasons. By partitioning the variation in bacterial community structure, we could assess that environmental and meteorological conditions, including variability between cities and seasons, were the major determinants of the observed variation in bacterial community structure, while chemical composition of atmospheric particulate matter (PM) had a minor contribution. Particularly, Ba, SO42− and Mg2+ concentrations were significantly correlated with microbial community structure, but it was not possible to assess whether they simply co-varied with seasonal shifts of bacterial inputs to the atmosphere, or their variation favoured specific taxa. Both local sources of bacteria and atmospheric dispersal were involved in the assembling of airborne microbial communities, as suggested, to the one side by the large abundance of bacteria typical of lagoon environments (Rhodobacterales) observed in spring air samples from Venice and to the other by the significant effect of wind speed in shaping airborne bacterial communities at all sites.

Effect of preservation method on the assessment of bacterial community structure in soil and water samples.

The methods used in sample preservation may affect the description of the microbial community structure by DNA-based techniques. This study aims at evaluating the effect of different storage conditions, including freezing, adding two liquid-based preservatives or simply storing samples with no preservative, on the structure of the microbial communities in aliquots of organic-rich soil and water samples as revealed by a terminal restriction fragment length polymorphisms. The results showed that the number of terminal restriction fragments (TRFs) detected in soil aliquots stored with LifeGuard(™) solution was significantly lower than that of samples analyzed immediately after sampling. Moreover, cluster and PCA analyses showed that soil aliquots stored using LifeGuard(™) clustered separately from those stored with the other methods. Conversely, soil and water aliquots stored with DMSO-EDTA-salt solution did not show either significant reduction in the number of TRFs or any change in the structure of the microbial community. Finally, the number of TRFs and the structure of microbial communities from soil aliquots stored with no preservative did not differ from those of aliquots analyzed immediately after sampling. Preservation methods should therefore be accurately evaluated before collecting samples that have to be stored for long time before DNA extraction.

Migratory connectivity and effects of winter temperatures on migratory behaviour of the European robin Erithacus rubecula: a continent‐wide analysis

Many partially migratory species show phenotypically divergent populations in terms of migratory behaviour, with climate hypothesized to be a major driver of such variability through its differential effects on sedentary and migratory individuals. Based on long-term (1947-2011) bird ringing data, we analysed phenotypic differentiation of migratory behaviour among populations of the European robin Erithacus rubecula across Europe. We showed that clusters of populations sharing breeding and wintering ranges varied from partial (British Isles and Western Europe, NW cluster) to completely migratory (Scandinavia and north-eastern Europe, NE cluster). Distance migrated by birds of the NE (but not of the NW) cluster decreased through time because of a north-eastwards shift in the wintering grounds. Moreover, when winter temperatures in the breeding areas were cold, individuals from the NE cluster also migrated longer distances, while those of the NW cluster moved over shorter distances. Climatic conditions may therefore affect migratory behaviour of robins, although large geographical variation in response to climate seems to exist.

Assessing costs of carrying geolocators using feather corticosterone in two species of aerial insectivore

Despite benefits of using light-sensitive geolocators to track animal movements and describe patterns of migratory connectivity, concerns have been raised about negative effects of these devices, particularly in small species of aerial insectivore. Geolocators may act as handicaps that increase energetic expenditure, which could explain reported effects of geolocators on survival. We tested this ‘Energetic Expenditure Hypothesis’ in 12 populations of tree swallows (Tachycineta bicolor) and barn swallows (Hirundo rustica) from North America and Europe, using measurements of corticosterone from feathers (CORTf) grown after deployment of geolocators as a measure of physiology relevant to energetics. Contrary to predictions, neither among- (both species) nor within-individual (tree swallows only) levels of CORTf differed with respect to instrumentation. Thus, to the extent that CORTf reflects energetic expenditure, geolocators apparently were not a strong handicap for birds that returned post-deployment. While this physiological evidence suggests that information about migration obtained from returning geolocator-equipped swallows is unbiased with regard to levels of stress, we cannot discount the possibility that corticosterone played a role in reported effects of geolocators on survival in birds, and suggest that future studies relate corticosterone to antecedent factors, such as reproductive history, and to downstream fitness costs.

A Trade-Off between Reproduction and Feather Growth in the Barn Swallow (Hirundo rustica)

Physiological trade-offs mediated by limiting energy, resources or time constrain the simultaneous expression of major functions and can lead to the evolution of temporal separation between demanding activities. In birds, plumage renewal is a demanding activity, which accomplishes fundamental functions, such as allowing thermal insulation, aerodynamics and socio-sexual signaling. Feather renewal is a very expensive and disabling process, and molt is often partitioned from breeding and migration. However, trade-offs between feather renewal and breeding have been only sparsely studied. In barn swallows (Hirundo rustica) breeding in Italy and undergoing molt during wintering in sub-Saharan Africa, we studied this trade-off by removing a tail feather from a large sample of individuals and analyzing growth bar width, reflecting feather growth rate, and length of the growing replacement feather in relation to the stage in the breeding cycle at removal and clutch size. Growth bar width of females and length of the growing replacement feather of both sexes were smaller when the original feather had been removed after clutch initiation. Importantly, in females both growth bar width and replacement feather length were negatively predicted by clutch size, and more strongly so for large clutches and when feather removal occurred immediately after clutch completion. Hence, we found strong, coherent evidence for a trade-off between reproduction, and laying effort in particular, and the ability to generate new feathers. These results support the hypothesis that the derived condition of molting during wintering in long-distance migrants is maintained by the costs of overlapping breeding and molt.