Alessandro Tanferna

Individual improvements and selective mortality shape lifelong migratory performance

Billions of organisms, from bacteria to humans, migrate each year and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1–27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

Raptor Nest Decorations Are a Reliable Threat Against Conspecifics

Black kite nest decorations are honest signals of individual and territory quality. Individual quality is often signaled by phenotypic flags, such as bright plumage patches in birds. Extended phenotype signals can similarly show quality, but in these cases the signals are external to the individual, often taking the form of objects scavenged from the environment. Through multiple manipulative experiments, we showed that objects used for nest decoration by a territorial raptor, the black kite (Milvus migrans), act as reliable threats to conspecifics, revealing the viability, territory quality, and conflict dominance of the signaler. Our results suggest that animal-built structures may serve as signaling devices much more frequently than currently recognized.

Carotenoids and Skin Coloration in a Social Raptor

Abstract The outcome of social and sexual competition in animals is typically mediated through the expression of body traits. Conspicuous characters such as yellow, orange, and red colorations in skin, scales, and feathers are often posited as quality-dependent signals, because such colors are made of dietary carotenoids and their use for signaling conflicts with health functions. Raptors often lack brightly colored feathers but most diurnal species display intense orange and yellow hues in the cere and legs. Here we test the hypothesis that integument coloration functions as a signal of status in wild raptors, revealing availability of carotenoid pigments. As study model we used the Black Kite (Milvus migrans), a highly social, long-lived, and sexually monogamous Accipitriform. Regular trapping of adults throughout the breeding season revealed that circulating carotenoid levels were highest in breeding males, whereas breeding females and floaters showed moderate and statistically similar carotenoid titer...

No effect of satellite tagging on survival, recruitment, longevity, productivity and social dominance of a raptor, and the provisioning and condition of its offspring

Summary The deployment of electronic devices on animals is rapidly expanding and producing leapfrog advances in ecological knowledge. Even though their effects on the ecology and behaviour of the marked subjects are potentially important, <10% of the studies are accompanied by an evaluation of impact, and comprehensive, long-term assessments have been few. Therefore, there is an urgent need to test for impacts, especially for tags that are heavy and deployed for long time periods, such as satellite transmitters. We marked 110 individuals of a medium-sized, migratory raptor, the black kite Milvus migrans, with GPS satellite tags, representing about 4% of the body mass and attached as backpacks through a Teflon harness. Tagged individuals were compared to control animals of similar sex, age and breeding status for a large number of behavioural, condition-related and ecological traits. Despite a sample size two- to threefold greater than most previous assessments that reported significant impacts, there was no detectable difference between tagged and control individuals in key vital rates such as survival probability, longevity, recruitment, age of first breeding, reproductive performance and timing of breeding. Tagged and untagged kites showed similar social dominance during fights over food and a similar capability to provision nestlings, which prevented carry-over effects on the stress levels and condition of their offspring. Synthesis and applications. Radio-marking studies are growing exponentially in the current ‘movement ecology era’, and impact assessments will be ever more important. In principle, tags of up to 4% mass-load can be deployed without apparent harm on some avian soaring species, but impacts should be properly evaluated on a case-by-case basis. Resilient species for which impacts seem weak could be used as early warning systems for trials of new devices: if impacts are observed, they are likely to be even greater on more vulnerable species. Finally, individual fatalities caused by marking should be taken into serious account, but comprehensively evaluated in the light of broader population-level impacts. Future initiatives to minimize tagging impacts could include more stringent licensing criteria enforcing attendance at training courses or incorporation of impact evaluations into study designs, increased availability of training courses for tagging, and enhanced sharing of information through blogs, workshops or specialized journal sections.

Simultaneous analysis of multiple PCR amplicons enhances capillary SSCP discrimination of MHC alleles

Major histocompatibility complex (MHC) genotyping still remains one of the most challenging issues for evolutionary ecologists. To date, none of the proposed methods have proven to be perfect, and all provide both important pros and cons. Although denaturing capillary electrophoresis has become a popular alternative, allele identification commonly relies upon conformational polymorphisms of two single‐stranded DNA molecules at the most. Using the MHC class II (β chain, exon 2) of the black kite (Aves: Accipitridae) as our model system, we show that the simultaneous analysis of overlapping PCR amplicons from the same target region substantially enhances allele discrimination. To cover this aim, we designed a multiplex PCR capable to generate four differentially sized and labeled amplicons from the same allele. Informative peaks to assist allele calling then fourfold those generated by the analysis of single PCR amplicons. Our approach proved successful to differentiate all the alleles (N=13) isolated from eight unrelated birds at a single optimal run temperature and electrophoretic conditions. In particular, we emphasize that this approach may constitute a straightforward and cost‐effective alternative for the genotyping of single or duplicated MHC genes displaying low to moderate sets of divergent alleles.

Ambient temperature, body condition and sibling rivalry explain feather corticosterone levels in developing black kites

Summary In birds, the steroid hormone corticosterone (CORT) is considered a major mediator in a number of physiological mechanisms and behaviours critical for the regulation of an organisms energy balance. However, the question of whether the way in which circulating plasma CORT is incorporated into feathers actually reflects this regulation, and consequently whether feather CORT (CORT-F) measures allow to make inferences on past levels of energetic demands (also known as the allostatic load), remains unclear. While previous studies have yielded promising results, the technique still wants further study and validation in a wider range of bird species, across life-history stages and under different ecological situations. Here, we tested whether CORT-F levels in a sample of 427 nestling black kites (Milvus migrans) reflected interindividual variation in a number of environmental, social and physiological variables known to elevate allostatic load during development. We found that nestlings exposed to low ambient temperatures exhibited high CORT-F, suggesting that feathers registered the expected rise in circulating CORT levels inducing thermogenesis in response to cold stress. CORT-F was also negatively related to body condition, supporting the notion that allostasis becomes less affordable as energy stores become depleted. Finally, CORT-F also reflected brood hierarchy rank, with subordinate chicks exhibiting the highest levels, followed by first-hatched (dominant) chicks and lastly singleton nestlings. Moreover, CORT-F levels in nestlings from multiple-chick broods (but not in singletons) declined with age, mirroring the dynamics of establishment and stabilization of sibling hierarchies in black kites. Altogether, our results underscore the potential of using CORT-F to infer allostatic load in wild avian populations and their potential power as indicator tools in conservation biology.

Does avian conspicuous colouration increase or reduce predation risk

Animals often announce their unprofitability to predators through conspicuous coloured signals. Here we tested whether the apparently conspicuous colour designs of the four European Coraciiformes and Upupiformes species may have evolved as aposematic signals, or whether instead they imply a cost in terms of predation risk. Because previous studies suggested that these species are unpalatable, we hypothesized that predators could avoid targeting them based on their colours. An experiment was performed where two artificial models of each bird species were exposed simultaneously to raptor predators, one painted so as to resemble the real colour design of these birds, and the other one painted using cryptic colours. Additionally, we used field data on the black kite’s diet to compare the selection of these four species to that of other avian prey. Conspicuous models were attacked in equal or higher proportions than their cryptic counterparts, and the attack rate on the four species increased with their respective degree of contrast against natural backgrounds. The analysis of the predator’s diet revealed that the two least attacked species were negatively selected in nature despite their abundance. Both conspicuous and cryptic models of one of the studied species (the hoopoe) received fewer attacks than cryptic models of the other three species, suggesting that predators may avoid this species for characteristics other than colour. Globally, our results suggest that the colour of coraciiforms and upupiforms does not function as an aposematic signal that advises predators of their unprofitability, but also that conspicuous colours may increase predation risk in some species, supporting thus the handicap hypothesis.

Different location sampling frequencies by satellite tags yield different estimates of migration performance: pooling data requires a common protocol.

Background Migration research is in rapid expansion and increasingly based on sophisticated satellite-tracking devices subject to constant technological refinement, but is still ripe with descriptive studies and in need of meta-analyses looking for emergent generalisations. In particular, coexistence of studies and devices with different frequency of location sampling and spatial accuracy generates doubts of data compatibility, potentially preventing meta-analyses. We used satellite-tracking data on a migratory raptor to: (1) test whether data based on different location sampling frequencies and on different position subsampling approaches are compatible, and (2) seek potential solutions that enhance compatibility and enable eventual meta-analyses. Methodology/Principal Findings We used linear mixed models to analyse the differences in the speed and route length of the migration tracks of 36 Black kites (Milvus migrans) satellite-tagged with two different types of devices (Argos vs GPS tags), entailing different regimes of position sampling frequency. We show that different location sampling frequencies and data subsampling approaches generate large (up to 33%) differences in the estimates of route length and migration speed of this migratory bird. Conclusions/Significance Our results show that the abundance of locations available for analysis affects the tortuosity and realism of the estimated migration path. To avoid flaws in future meta-analyses or unnecessary loss of data, we urge researchers to reach an agreement on a common protocol of data presentation, and to recognize that all transmitter-based studies are likely to underestimate the actual distance traveled by the marked animal. As ecological research becomes increasingly technological, new technologies should be matched with improvements in analytical capacity that guarantee data compatibility.

Migration by breeders and floaters of a long-lived raptor: implications for recruitment and territory quality

Animal migration is receiving increasing research attention through ever more sophisticated tracking technologies, but the difficulty of trapping nonbreeding floaters has prevented comprehensive tracking studies of how migration varies in young breeders and floaters and whether this has consequences for recruitment (i.e. the transition from floating to breeding). To fill this gap, we satellite-GPS tracked young black kites, Milvus migrans , which start to breed when 1–7 years old. In the prebreeding migration, floaters departed and arrived later than breeders, travelled faster with fewer days at stopovers, as if in a hurry, and suffered more from cross-winds. Survival, recruitment, the territory quality and offspring production of the first reproductive attempt, as well as eventual longevity, declined rapidly with small departure delays. The high payoffs for small gains in timing set young kites on a race for early arrival: individuals improved their departure through early life and late migrants were progressively removed from the population or lingered as old floaters. As a result, individual improvements and selective mortality caused each cohort to progressively split after 3 years of age between a vanishing tail of late floaters and a body of early travelling individuals that then shaped the migratory traits of the adult population. Thus, migration in early life acted as a demographic bottleneck that filtered the transition to the next stage of the life cycle through a carryover effect that linked events operating on different continents.

Effects of Ontogeny, Diel Rhythms, and Environmental Variation on the Adrenocortical Physiology of Semialtricial Black Kites (Milvus migrans)

We examined whether hypothalamic-pituitary-adrenal axis activity in the nestlings of a semialtricial raptor, the black kite (Milvus migrans), varied with advancing age, throughout the day, and in response to a number of socioecological factors presumed to affect allostatic load. Both baseline corticosterone (CORT) titers and maximum CORT levels during 30 min of handling and restraint augmented across all sampled ages, suggesting that nestlings’ energetic demands and capacity to respond to perturbations increase progressively throughout development. CORT secretion also peaked in the early morning, reached minimum levels in the central hours of the day, and increased again before dusk, suggesting a possible role of CORT in the regulation of activity-inactivity patterns. Finally, nestlings raised in a year of low marsh inundation, implying lower food availability and heightened allostatic loads, exhibited higher adrenocortical responsiveness to stress than nestlings raised in years of intermediate or high flooding. The nondetectable effect of other socioecological variables, such as territory quality, temperature, or brood order, suggests that parents may be able to buffer their nestlings from adverse environmental conditions or that the effect of such factors may have been obscured by selective mortality operating before sampling. We propose that future studies increase the simultaneous use of complementary techniques (fecal sampling, feather analysis) to reach firmer and more comprehensive conclusions, especially for planning the management and conservation of sensitive species.