Jacopo G. Cecere

Polymorphism at the Clock gene predicts phenology of long-distance migration in birds

Dissecting phenotypic variance in life history traits into its genetic and environmental components is at the focus of evolutionary studies and of pivotal importance to identify the mechanisms and predict the consequences of human‐driven environmental change. The timing of recurrent life history events (phenology) is under strong selection, but the study of the genes that control potential environmental canalization in phenological traits is at its infancy. Candidate genes for circadian behaviour entrained by photoperiod have been screened as potential controllers of phenological variation of breeding and moult in birds, with inconsistent results. Despite photoperiodic control of migration is well established, no study has reported on migration phenology in relation to polymorphism at candidate genes in birds. We analysed variation in spring migration dates within four trans‐Saharan migratory species (Luscinia megarhynchos; Ficedula hypoleuca; Anthus trivialis; Saxicola rubetra) at a Mediterranean island in relation to Clock and Adcyap1 polymorphism. Individuals with larger number of glutamine residues in the poly‐Q region of Clock gene migrated significantly later in one or, respectively, two species depending on sex and whether the within‐individual mean length or the length of the longer Clock allele was considered. The results hinted at dominance of the longer Clock allele. No significant evidence for migration date to covary with Adcyap1 polymorphism emerged. This is the first evidence that migration phenology is associated with Clock in birds. This finding is important for evolutionary studies of migration and sheds light on the mechanisms that drive bird phenological changes and population trends in response to climate change.

Pelagic seabird flight patterns are consistent with a reliance on olfactory maps for oceanic navigation

Homing studies have provided tantalizing evidence that the remarkable ability of shearwaters (Procellariiformes) to pinpoint their breeding colony after crossing vast expanses of featureless open ocean can be attributed to their assembling cognitive maps of wind-borne odours but crucially, it has not been tested whether olfactory cues are actually used as a system for navigation. Obtaining statistically important samples of wild birds for use in experimental approaches is, however, impossible because of invasive sensory manipulation. Using an innovative non-invasive approach, we provide strong evidence that shearwaters rely on olfactory cues for oceanic navigation. We tested for compliance with olfactory-cued navigation in the flight patterns of 210 shearwaters of three species (Corys shearwaters, Calonectris borealis, North Atlantic Ocean, Scopolis shearwaters, C. diomedea Mediterranean Sea, and Cape Verde shearwaters, C. edwardsii, Central Atlantic Ocean) tagged with high-resolution GPS loggers during both incubation and chick rearing. We found that most (69%) birds displayed exponentially truncated scale-free (Lévy-flight like) displacements, which we show are consistent with olfactory-cued navigation in the presence of atmospheric turbulence. Our analysis provides the strongest evidence yet for cognitive odour map navigation in wild birds. Thus, we may reconcile two highly disputed questions in movement ecology, by mechanistically connecting Lévy displacements and olfactory navigation. Our approach can be applied to any species which can be tracked at sufficient spatial resolution, using a GPS logger.

Nectar: an energy drink used by European songbirds during spring migration

Nectar exploitation by European birds mainly refers to passerines feeding on exotic plants, although some recent studies described nectar-feeding by trans-Saharan passerines on local plants. We examined which birds and plants are involved in nectar consumption and investigated the consequences of nectar use on plasma blood glucose concentrations during spring migration at a stopover site in the central Mediterranean. We recorded 12 opportunistic nectar-feeding species, with Sylvia warblers in particular showing a marked nectarivory, and 6 plants used by birds, no one of which shows typical “bird flowers” features. Moreover, we demonstrated that nectar uptake led to an increase in plasma glucose concentrations and that nectar was drunk not only by birds in poor physical condition. The nectar consumption is fully in accordance with time-minimising migration models, allowing birds to obtain water and energy at stopover sites in a short time: nectar is easy to find and quick to digest.ZusammenfassungNektarkonsum durch europäische Singvögel wurde bisher vornehmlich an exotischen Pflanzen beobachtet. Jüngere Studien beschreiben aber auch Nektarkonsum durch trans-Sahar Zugvögel an einheimischen Pflanzen. In dieser Studie untersuchten wir während des Frühlingszuges an einem Rastplatz im zentralen Mittelmeerraum, welche Vogelarten welche Pflanzen für den Nektarkonsum nutzen, und welche Auswirkungen die Nektaraufnahme auf die Plasmakonzentration der Glukose hat. 12 Arten, insbesondere Grasmücken, tranken Nektar an insgesamt sechs Pflanzenarten, von denen keine die typischen Merkmale der Ornithophilie zeigte. Die Nektaraufnahme führte zu einem Anstieg der Plasmaglukosekonzentration und wurde vor allem von Vögeln in schlechter körperlicher Verfassung genutzt. Nektar ist eine Energiequelle mit vielen Vorteilen: sie ist schnell zu finden, rasch aufzunehmen und leicht zu verdauen. Dieser Vorteil, Wasser und Energie in kurzer Zeit aufzunehmen, reduziert die Zeit, die Zugvögel an einem Rastplatz verbringen müssen und unterstützt das Zeit-Minimierungsmodell.

The Lévy flight foraging hypothesis in a pelagic seabird

Lévy flight foraging represents an innovative paradigm for the analysis of animal random search by including models of heavy-tailed distribution of move length, which complements the correlated random walk paradigm that is founded on Brownian walks. Theory shows that the efficiency of the different foraging tactics is a function of prey abundance and dynamics with Lévy flight being especially efficient in poor prey fields. Lévy flights have been controversial in some quarters, because they previously have been wrongly ascribed to many species through the employment of inappropriate statistical techniques and by misunderstanding movement pattern data. More recent studies using state-of-the-art statistical tools have, however, provided seemingly compelling evidence for Lévy flights. In this study, we employ these maximum-likelihood methods and their Bayesian equivalents by analysing both turning angles and move length distributions. We tested, for compliance with Lévy flight foraging, a set of 77 independent foraging trajectories of Corys shearwaters Calonectris diomedea diomedea. Birds were tagged with high-resolution GPS loggers in two Mediterranean colonies (Linosa and Tremiti) during both incubation and chick rearing. We found that the behaviour of six birds was fitted by a correlated random walk; the movement of 32 birds was better represented by adaptive correlated random walks by switching from intensive to extensive searches; and the trajectories of 36 birds were fitted by a Lévy flight pattern of movement. The probability of performing Lévy flights was higher for trips during chick provisioning when shearwaters were forced to forage in suboptimal areas. This study supports Lévy flight foraging as an appropriate framework to analyse search tactics in this pelagic bird species and highlights that the adoption of a given search strategy is a function of biological and ecological constraints.

Movement patterns and habitat use during incubation and chick-rearing of Cory's shearwaters (Calonectris diomedea diomedea) (Aves: Vertebrata) from Central Mediterranean: influence of seascape and breeding stage

Abstract We analysed the patterns of movement and habitat use of Corys shearwaters (Calonectris diomedea diomedea) from two colonies in the central Mediterranean Sea: the island of Linosa and the Tremiti Archipelago. The colony of Linosa is placed in a rather pelagic environment, being about 160 km distant from the coasts of both Sicily and Tunisia, while the colony of Tremiti is rather near to the coast of the Adriatic Sea, being only 25 km from the Italian coast. Field work during incubation was carried out at both colonies and throughout chick-rearing only at Linosa. We aimed to test first whether birds from the two colonies differ significantly in habitat use, and secondly whether constraints during incubation and chick-rearing lead birds to explore different habitats. Trip duration was correlated with the farthest distance covered in both colonies and, for Linosa birds, it decreased at the start of chick-rearing but increased later. During incubation the expanse of explored areas did not differ between the colonies, but for Tremiti these were generally characterized by higher average primary production and shallower waters than those for Linosa. Furthermore, during the incubation period Linosa birds explored areas with higher values of primary production and shallower waters than during chick-rearing. Chick-rearing is therefore likely to constrain birds to use sub-optimal areas closer to their colony due to the intense pressures of chick provisioning. Our data indicate that conservation efforts should therefore aim not only to protect the best foraging areas but also to conserve areas closer to the colonies, which will be profitable enough to provide adult birds with sufficient food for chick-rearing.

Genomic evidence of demographic fluctuations and lack of genetic structure across flyways in a long distance migrant, the European turtle dove

BackgroundUnderstanding how past climatic oscillations have affected organismic evolution will help predict the impact that current climate change has on living organisms. The European turtle dove, Streptopelia turtur, is a warm-temperature adapted species and a long distance migrant that uses multiple flyways to move between Europe and Africa. Despite being abundant, it is categorized as vulnerable because of a long-term demographic decline. We studied the demographic history and population genetic structure of the European turtle dove using genomic data and mitochondrial DNA sequences from individuals sampled across Europe, and performing paleoclimatic niche modelling simulations.ResultsOverall our data suggest that this species is panmictic across Europe, and is not genetically structured across flyways. We found the genetic signatures of demographic fluctuations, inferring an effective population size (Ne) expansion that occurred between the late Pleistocene and early Holocene, followed by a decrease in the Ne that started between the mid Holocene and the present. Our niche modelling analyses suggest that the variations in the Ne are coincident with recent changes in the availability of suitable habitat.ConclusionsWe argue that the European turtle dove is prone to undergo demographic fluctuations, a trait that makes it sensitive to anthropogenic impacts, especially when its numbers are decreasing. Also, considering the lack of genetic structure, we suggest all populations across Europe are equally relevant for conservation.

Clock gene polymorphism, migratory behaviour and geographic distribution: a comparative study of trans‐Saharan migratory birds

Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate ‘circadian clock’ genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans‐Saharan migratory bird species, we investigated the relationships between species‐level genetic variation at two candidate genes, Clock and Adcyap1, and species’ traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in ‘circadian clock’ genotype frequencies, Clock allele size increased with breeding latitude across species. However, early‐ and late‐migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long‐distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long‐distance migratory species, likely resulting from the time constraints imposed by late spring migration.

Lévy patterns in seabirds are multifaceted describing both spatial and temporal patterning.

BackgroundThe flight patterns of albatrosses and shearwaters have become a touchstone for much of Lévy flight research, spawning an extensive field of enquiry. There is now compelling evidence that the flight patterns of these seabirds would have been appreciated by Paul Lévy, the mathematician after whom Lévy flights are named. Here we show that Lévy patterns (here taken to mean spatial or temporal patterns characterized by distributions with power-law tails) are, in fact, multifaceted in shearwaters being evident in both spatial and temporal patterns of activity.ResultsWe tested for Lévy patterns in the at-sea behaviours of two species of shearwater breeding in the North Atlantic Ocean (Calonectris borealis) and the Mediterranean sea (C. diomedea) during their incubating and chick-provisioning periods. We found that distributions of flight durations, on/in water durations and inter-dive time-intervals have power-law tails and so bear the hallmarks of Lévy patterns.ConclusionsThe occurrence of these statistical laws is remarkable given that bird behaviours are strongly shaped by an individual’s motivational state and by complex environmental interactions. Our observations could take Lévy patterns as models of animal behaviour to a new level by going beyond the characterisation of spatial movements to characterise how different behaviours are interwoven throughout daily animal life.

Candidate genes have sex-specific effects on timing of spring migration and moult speed in a long-distance migratory bird

Abstract The timing of major life-history events, such as migration and moult, is set by endogenous circadian and circannual clocks, that have been well characterized at the molecular level. Conversely, the genetic sources of variation in phenology and in other behavioral traits have been sparsely addressed. It has been proposed that inter-individual variability in the timing of seasonal events may arise from allelic polymorphism at phenological candidate genes involved in the signaling cascade of the endogenous clocks. In this study of a long-distance migratory passerine bird, the willow warbler Phylloscopus trochilus, we investigated whether allelic variation at 5 polymorphic loci of 4 candidate genes (Adcyap1, Clock, Creb1, and Npas2), predicted 2 major components of the annual schedule, namely timing of spring migration across the central Mediterranean sea and moult speed, the latter gauged from ptilochronological analyses of tail feathers moulted in the African winter quarters. We identified a novel Clock gene locus (Clock region 3) showing polyQ polymorphism, which was however not significantly associated with any phenotypic trait. Npas2 allele size predicted male (but not female) spring migration date, with males bearing longer alleles migrating significantly earlier than those bearing shorter alleles. Creb1 allele size significantly predicted male (but not female) moult speed, longer alleles being associated with faster moult. All other genotype–phenotype associations were statistically non-significant. These findings provide new evidence for a role of candidate genes in modulating the phenology of different circannual activities in long-distance migratory birds, and for the occurrence of sex-specific candidate gene effects.

Home, dirty home: effect of old nest material on nest-site selection and breeding performance in a cavity-nesting raptor

Abstract The quality of a breeding site may have major fitness consequences. A fundamental step to understanding the process of nest-site selection is the identification of the information individuals use to choose high-quality nest sites. For secondary cavity-nesting bird species that do not add nest lining material, organic remains (faeces, pellets) accumulated inside nest cavities during previous breeding events may be a cue for high-quality nest-sites, as they contain information about past successful breeding and may improve thermal insulation of eggs during incubation. However, cavities in which breeding was successful might also contain more nest-dwelling ectoparasites than unoccupied cavities, offering an incentive for prospective parents to avoid them. We exposed breeding cavity-nesting lesser kestrels (Falco naumanni) to nestbox dyads consisting of a dirty (with a thick layer of organic substrate) and a clean nestbox (without organic material). Dirty nestboxes were strongly preferred, being occupied earlier and more frequently than clean ones. Hatching success in dirty nestboxes was significantly higher than in clean ones, suggesting a positive effect of organic nest material on incubation efficiency, while nestbox dirtiness did not significantly affect clutch and brood size. Nestlings from dirty nestboxes had significantly higher ectoparasite load than those from clean nestboxes soon after egg hatching, but this difference was not evident a few days later. Nest substrate did not significantly affect nestling growth. We concluded that nest substrate is a key driver of nest-site choice in lesser kestrels, although the adaptive value of such a strong preference appears elusive and may be context-dependent.