Spring phenology of ecological productivity contributes to the use of looped migration strategies by birds

Migration is a common strategy used by birds that breed in seasonal environments. The patterns and determinants of migration routes, however, remain poorly understood. Recent empirical analyses have demonstrated that the locations of two North America migration flyways (eastern and western) shift seasonally, reflecting the influence of looped migration strategies. For the eastern but not western flyway, seasonal variation in atmospheric circulation has been identified as an explanation. Here, we test an alternative explanation based on the phenology of ecological productivity, which may be of greater relevance in western North America, where phenology is more broadly dictated by elevation. Migrants in the western flyway selected lower-elevation spring routes that were wetter, greener and more productive, and higher-elevation autumn routes that were less green and less productive, but probably more direct. Migrants in the eastern flyway showed little season variation but maintained associations with maximum regional greenness. Our findings suggest the annual phenology of ecological productivity is associated with en route timing in both flyways, and the spring phenology of ecological productivity contributes to the use of looped strategies in the western flyway. This fine-tuned spatial synchronization may be disrupted when changing climate induces a mismatch between food availability and needs.     

Avian eggshell thickness: scaling and maximum body mass in birds

The avian eggshell represents a highly evolved structure adapted to the physiological requirements of the embryo and the potential fracturing forces it is exposed to during incubation. Given its many roles, it is not surprising that the eggshell is also central to the current hypothesis about maximum avian body mass. Eggshell thickness ( L ) and strength has historically been scaled as a function of initial egg mass (IEM). However, maximum incubator mass (IM) is likely a better indicator of the forces the shell must be selected to withstand during incubation. We compare the results of analyses of L ² (an indicator of shell strength) as a function of IEM and IM. We conclude from IM scaling that megapode and kiwi eggshells are not thin but rather are thicker than expected and in general birds with a clutch size of 1 have thicker shells, and further, that reversed sexual dimorphism in the large, particularly extinct birds may be a strategy to avoid shell breakage during incubation of the largest eggs without creating a shell so thick as to inhibit hatching.     

Optimal moult strategies in migratory birds

Avian migration, which involves billions of birds flying vast distances, is known to influence all aspects of avian life. Here we investigate how birds fit moult into an annual cycle determined by the need to migrate. Large variation exists in moulting patterns in relation to migration: for instance, moult can occur after breeding in the summer or after arrival in the wintering quarters. Here we use an optimal annual routine model to investigate why this variation exists. The modelled bird's decisions depend on the time of year, its energy reserves, breeding status, experience, flight feather quality and location. Our results suggest that the temporal and spatial variations in food are an important influence on a migratory bird's annual cycle. Summer moult occurs when food has a high peak on the breeding site in the summer, but it is less seasonal elsewhere. Winter moult occurs if there is a short period of high food availability in summer and a strong winter peak at different locations (i.e. the food is very seasonal but in opposite phase on these areas). This finding might explain why only long-distance migrants have a winter moult.     

Moult in the Loggerhead Shrike Lanius ludovicianus is influenced by sex,latitude and migration

We investigated moult strategies in Loggerhead Shrikes by examining first prebasic or preformative moult patterns and by assessing the general location where individual feathers were grown using stable hydrogen isotope (δ²H) analysis. We tested the relative importance of factors known to impact moult timing and pattern, including age, sex, body size, food availability and migration. Migratory Shrikes showed evidence of suspended moult, in which feathers are moulted on both the breeding and the non‐breeding grounds with a suspension of moult during migration. Extent of moult was best explained by sex, longitude, migratory behaviour and breeding‐ground latitude. Male Hatch Year (HY) Shrikes replaced more feathers on the breeding grounds prior to migration than did HY females and moulted more extensively on the breeding grounds than did females. Non‐migratory HY Shrikes underwent a more extensive preformative moult than migratory HY Shrikes. Individuals in more southerly migratory populations moulted more extensively on the breeding grounds than did those breeding further north. Our data also indicate that individuals in the northeastern populations moulted more extensively on the breeding grounds than did those in the north and southwest. Our study underlines the complex structure and variation in moult possible within species, revealing surprising levels of differentiation between sexes and age cohorts, linked to environmental factors on the breeding grounds. Our study highlights the utility of an intrinsic marker, specifically δ²H analysis, to test hypotheses regarding the evolutionary and ecological forces driving moult. Although the methodology has not commonly been applied to this area of research, our results indicate that it can provide unprecedented insight into inter‐ and intra‐specific adaptive response to constraints, whereby individuals maximize fitness.     

Autumn bird migration phenology: A potpourri of wind,precipitation and temperature effects

Climate change has caused a clear and univocal trend towards advancement in spring phenology. Changes in autumn phenology are much more diverse, with advancement, delays, and ‘no change' all occurring frequently. For migratory birds, patterns in autumn migration phenology trends have been identified based on ecological and life‐history traits. Explaining interspecific variation has nevertheless been challenging, and the underlying mechanisms have remained elusive. Radar studies on non‐species‐specific autumn migration intensity have repeatedly suggested that there are strong links with weather. In long‐term species‐specific studies, the variance in autumn migration phenology explained by weather has, nevertheless, been rather low, or a relationship was even lacking entirely. We performed a spatially explicit time window analysis of weather effects on mean autumn passage of four trans‐Saharan and six intra‐European passerines to gain insights into this apparent contradiction. We analysed data from standardized daily captures at the Heligoland island constant‐effort site (Germany), in combination with gridded daily temperature, precipitation and wind data over a 55‐year period (1960–2014), across northern Europe. Weather variables at the breeding and stopover grounds explained up to 80% of the species‐specific interannual variability in autumn passage. Overall, wind conditions were most important. For intra‐European migrants, wind was even twice as important as either temperature or precipitation, and the pattern also held in terms of relative contributions of each climate variable to the temporal trends in autumn phenology. For the trans‐Saharan migrants, however, the pattern of relative trend contributions was completely reversed. Temperature and precipitation had strong trend contributions, while wind conditions had only a minor impact because they did not show any strong temporal trends. As such, understanding species‐specific effects of climate on autumn phenology not only provides unique insights into each species' ecology but also how these effects shape the observed interspecific heterogeneity in autumn phenological trends.     

Altitudinal migration by birds: a review of the literature and a comprehensive list of species

Altitudinal migration is the seasonal altitudinal movement of birds from breeding areas to non‐breeding or wintering areas at different elevations. Although this type of migration is widely reported, questions remain concerning the number of species that perform altitudinal migration, possible variation among different taxa and geographic locations in the extent of altitudinal migration, and the foraging guilds of altitudinal migrants. We conducted an extensive bibliographic survey and compiled a list of altitudinal migrant birds worldwide. We characterized species in terms of their foraging guilds because the spatial distribution of food resources along altitudinal gradients is often evoked as a driver of bird altitudinal migration. We identified 1238 species of altitudinal migrants, ~10% of the ~10,000 extant species of birds. We found a strong geographic bias in publications focusing on avian altitudinal migration toward the United States and Costa Rica, and a paucity of studies in megadiverse regions such as the Afrotropical and Indomalayan realms, and areas in the Neotropics other than Costa Rica. We also found that most species of altitudinal migrants were invertivores rather than frugivores or nectarivores. This general pattern held true for all zoogeographic realms except the Neotropics, where nectarivores and frugivores predominated among altitudinal migrants. The prevalence of invertivore birds among altitudinal migrants is not unexpected because this is the most common foraging guild among birds worldwide. Overall, we found no prevalence of any specific foraging guild among altitudinal migrants across zoogeographic regions. The results of studies to date suggest that altitudinal migration by birds may be driven by a number of factors, including access to increased food resources for breeding or molting, weather conditions, and mating and nesting opportunities. However, to better understand the mechanisms underlying altitudinal migration, broadening the geographic scope of studies is paramount, with additional study of altitudinal migration especially needed in the megadiverse tropical regions of sub‐Saharan Africa, Southeast Asia, and South America.     

Mechanical and structural adaptations to migration in the flight feathers of a Palaearctic passerine

Current avian migration patterns in temperate regions have been developed during the glacial retreat and subsequent colonization of the ice‐free areas during the Holocene. This process resulted in a geographic gradient of greater seasonality as latitude increased that favoured migration‐related morphological and physiological (co)adaptations. Most evidence of avian morphological adaptations to migration comes from the analysis of variation in the length and shape of the wings, but the existence of intra‐feather structural adjustments has been greatly overlooked despite their potential to be under natural selection. To shed some light on this question, we used data from European robins Erithacus rubecula overwintering in Campo de Gibraltar (Southern Iberia), where sedentary robins coexist during winter with conspecifics showing a broad range of breeding origins and, hence, migration distances. We explicitly explored how wing length and shape, as well as several functional (bending stiffness), developmental (feather growth rate) and structural (size and complexity of feather components) characteristics of flight feathers, varied in relation to migration distance, which was estimated from the hydrogen stable isotope ratios of the summer‐produced tail feathers. Our results revealed that migration distance not only favoured longer and more concave wings, but also promoted primaries with a thicker dorsoventral rachis and shorter barb lengths, which, in turn, conferred more bending stiffness to these feathers. We suggest that these intra‐feather structural adjustments could be an additional, largely unnoticed, adaptation within the avian migratory syndrome that might have the potential to evolve relatively quickly to facilitate the occupation of seasonal environments.     

Phylogenetic analyses of the diversity of moult strategies in Sylviidae in relation to migration

Moult in birds is highly variable both within and among bird genera. The aim of the present study was to make an extended phylogenetic analysis of the diversity of moult strategies within Sylviidae in light of the recent phylogenies based on molecular data, and with the methodology of matched-pairs analysis. In the present study we analysed 141 sylviid taxa and, to improve character reconstruction, 22 outgroup taxa. The study could corroborate the earlier results that post-breeding moult is the ancestral state in Sylviidae. Migratory habits were found to be ancestral within Sylviidae but resident habits have evolved several times with a few reverse transitions back to migratory habits. Transitions in main moult strategy were significantly related to both migratory vs. resident habits and to migratory distance, giving support to the hypothesis that moult in the non-breeding season is related to migration as such and long-distance migration, respectively. Both resident and migratory taxa used minor alternative moult strategies besides the main moult strategy and such within-taxon flexibility might be a basal trait in Sylviidae. We investigated three variables that included minor strategies and found no relationship between these and migratory habits. However, two of these variables (the potential to interrupt moult and the occurrence of moult in both the post- and non-breeding seasons) were significantly related to migration distance. We conclude that migration patterns has some influence on the choice of moult strategy, and that flexibility in timing of moult is widespread within Sylviidae and might be a basal trait. We argue that such flexibility might be a prerequisite for changes in migratory strategies.     

Variable detours in long‐distance migration across ecological barriers and their relation to habitat availability at ground

Migration detours, the spatial deviation from the shortest route, are a widespread phenomenon in migratory species, especially if barriers must be crossed. Moving longer distances causes additional efforts in energy and time, and to be adaptive, this should be counterbalanced by favorable condition en route. We compared migration patterns of nightingales that travelled along different flyways from their European breeding sites to the African nonbreeding sites. We tested for deviations from shortest routes and related the observed and expected routes to the habitat availability at ground during autumn and spring migration. All individuals flew detours of varying extent. Detours were largest and seasonally consistent in western flyway birds, whereas birds on the central and eastern flyways showed less detours during autumn migration, but large detours during spring migration (eastern flyway birds). Neither migration durations nor the time of arrival at destination were related to the lengths of detours. Arrival at the breeding site was nearly synchronous in birds flying different detours. Flying detours increased the potential availability of suitable broad‐scale habitats en route only along the western flyway. Habitat availability on observed routes remained similar or even decreased for individuals flying detours on the central or the eastern flyway as compared to shortest routes. Thus, broad‐scale habitat distribution may partially explain detour performance, but the weak detour‐habitat association along central and eastern flyways suggests that other factors shape detour extent regionally. Prime candidate factors are the distribution of small suitable habitat patches at local scale as well as winds specific for the region and altitude.     

Where the wild birds go: explaining the differences in migratory destinations across terrestrial bird species

Given their large movement capacities, migratory birds have in principle a wide range of possible geographical locations for their breeding and non‐breeding destinations, yet each species migrates between consistent breeding and non‐breeding ranges. In this study, we use a macroecological approach to search for the general factors explaining the location of the seasonal ranges of migratory bird species across the globe. We develop a null model to test the hypotheses that access to resources, geographical distance, tracking of temperature, and habitat conditions (separately as well as considered together) have a major influence in the location of species’ migratory destinations, once each species’ geographical constraints are taken into account. Our results provide evidence for a trade‐off between costs associated with distance travelled and gains in terms of better access to resources. We also provide strong support to the hypotheses that all factors tested, with the exception of habitat, have a strong and additive effect on the global geography of bird migration. Indeed, our results indicate that species’ contemporary migratory destinations (i.e. the combination of their breeding and non‐breeding ranges) are such that they allow species to track a temperature regime throughout the year, to escape local competition and reach areas with better access to resources, and to minimise the spatial distance travelled, within the limitations imposed by the geographical location of each species. Our study thus sheds light on the mechanisms underpinning bird migration and provides a strong basis for predicting how migratory species will respond to future change.     

Circadian flight schedules in night-migrating birds caught on migration

Many species of migratory birds migrate in a series of solitary nocturnal flights. Between flights, they stop to rest and refuel for the next segment of their journey. The mechanism controlling this behaviour has long remained elusive. Here, we show that wild-caught migratory redstarts (Phoenicurus phoenicurus) are consistent in their flight scheduling. An advanced videographic system enabled us to determine the precise timing of flight activity in redstarts caught at a northern European stopover site during their return trip from Africa. Birds were held captive for three days in the absence of photoperiodic cues (constant dim light) and under permanent food availability. Despite the absence of external temporal cues, birds showed clear bimodal activity patterns: intense nocturnal activity alternating with diurnal foraging and resting periods. The onset of their migratory activity coincided with the time of local sunset and was individually consistent on consecutive nights. The data demonstrate that night-migrating birds are driven by autonomous circadian clocks entrained by sunset cues. This timekeeping system is probably the key factor in the overall control of nocturnal songbird migration.     

Senescence in relation to latitude and migration in birds

Senescence is the age‐related deterioration of the phenotype, explained by accumulation of mutations, antagonistic pleiotropy, free radicals or other mechanisms. I investigated patterns of actuarial senescence in a sample of 169 species of birds in relation to latitude and migration, by analysing longevity records adjusted for sampling effort, survival rate and body mass. Senescence might decrease at low latitudes because of elevated adult survival rates and generally slow life histories. Alternatively, the rate of senescence might increase at low latitudes because of the greater impact of biological interactions such as parasitism, predation and competition on fitness through differential effects of age‐specific mortality (e.g. because immunologically naïve young individuals and immuno‐senescent old individuals might die more frequently than individuals belonging to intermediate age classes). Bird migration entails extensive exercise twice annually, with migrants spending more time in benign environments with little abiotic mortality than residents, migrants having higher adult survival rate and lower annual fecundity than residents, and migrants suffering more from the consequences of oxidative stress than residents. The rate of senescence increased with latitude, as expected because of slow life histories at low latitudes. Independently, rate of senescence decreased with increasing migration distance. These findings were robust to control for potentially confounding effects of body mass, age of first reproduction and phenotypic similarity among species because of common descent.     

Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect

Recent evaluations of both temporal and spatial precision in bird migration have called for external cues in addition to the inherited programme defining the migratory journey in terms of direction, distance and fuelling behaviour along the route. We used juvenile European robins (Erithacus rubecula) to study whether geomagnetic cues affect fuel deposition in a medium-distance migrant by simulating a migratory journey from southeast Sweden to the wintering area in southern Spain. In the late phase of the onset of autumn migration, robins exposed to the magnetic treatment attained a lower fuel load than control birds exposed to the ambient magnetic field of southeast Sweden. In contrast, robins captured in the early phase of the onset of autumn migration all showed low fuel deposition irrespective of experimental treatment. These results are, as expected, the inverse of what we have found in similar studies in a long-distance migrant, the thrush nightingale (Luscinia luscinia), indicating that the reaction in terms of fuelling behaviour to a simulated southward migration varies depending on the relevance for the species. Furthermore, we suggest that information from the geomagnetic field act as an important external cue overriding the seasonal effect on fuelling behaviour in migratory birds.     

Corticosterone,testosterone and life-history strategies of birds

Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.     

The effects of long‐distance migration on the evolution of moult strategies in Western‐Palearctic passerines

Although feathers are the unifying characteristic of all birds, our understanding of the causes, mechanisms, patterns and consequences of the feather moult process lags behind that of other major avian life‐history phenomena such as reproduction and long‐distance migration. Migration, which evolved in many species of the temperate and arctic zones, requires high energy expenditure to endure long‐distance journeys. About a third of Western‐Palearctic passerines perform long‐distance migrations of thousands of kilometres each year using various morphological, physiological, biomechanical, behavioural and life‐history adaptations. The need to include the largely non‐overlapping breeding, long‐distance migration and feather moult processes within the annual cycle imposes a substantial constraint on the time over which the moult process can take place. Here, we review four feather‐moult‐related adaptations which, likely due to time constraints, evolved among long‐distance Western‐Palearctic migrants: (i) increased moult speed; (ii) increased overlap between moult and breeding or migration; (iii) decreased extent of plumage moult; and (iv) moult of part or all of the plumage during the over‐wintering period in the tropics rather than in the breeding areas. We suggest that long‐distance migration shaped the evolution of moult strategies and increased the diversity of these strategies among migratory passerines. In contrast to this variation, all resident passerines in the Western Palearctic moult immediately after breeding by renewing the entire plumage of adults and in some species also juveniles, while in other species juvenile moult is partial. We identify important gaps in our current understanding of the moult process that should be addressed in the future. Notably, previous studies suggested that the ancestral moult strategy is a post‐breeding summer moult in the Western Palearctic breeding areas and that moult during the winter evolved due to the scheduling of long‐distance migration immediately after breeding. We offer an alternative hypothesis based on the notion of southern ancestry, proposing that the ancestral moult strategy was a complete moult during the ‘northern winter’ in the Afro‐tropical region in these species, for both adults and juveniles. An important aspect of the observed variation in moult strategies relates to their control mechanisms and we suggest that there is insufficient knowledge regarding the physiological mechanisms that are involved, and whether they are genetically fixed or shaped by environmental factors. Finally, research effort is needed on how global climate changes may influence avian annual routines by altering the scheduling of major processes such as long‐distance migration and feather moult.     

On birds: scale effects in the neognath hindlimb and differences in the gross morphology of wings and hindlimbs

Scale effects on whole limb morphology (i.e. bones together with in situ overlying muscles) are well understood for the neognath forelimb. However, scale effects on neognath gross hindlimb morphology remain largely unexplored. To broaden our understanding of avian whole limb morphology, I investigated the scaling of hindlimb inertial properties in neognath birds, testing empirical scaling relationships against the model of geometric similarity. Inertial property data – mass, moment of inertia, centre of mass distance, and radius of gyration – were collected from 22 neognath species representing a wide range of locomotor specializations. When scaled against body mass, hindlimb inertial properties scale with positive allometry. Thus, in terms of morphology, larger bodied neognaths possess hindlimbs requiring disproportionately more energy to accelerate and decelerate relative to body mass than smaller bodied birds. When scaled against limb length, hindlimb inertial properties scale according to isometry. In the subclade Land Birds (sensu Hackett et al.), hindlimb inertial properties largely scale according to positive allometry. The contrasting results of positive allometry vs. isometry in neognaths are due to how hindlimb length scales against body mass. Negative allometry of hindlimb inertial properties, which would reduce terrestrial locomotion costs, would probably make the hindlimb susceptible to mechanical failure or too diminutive for its many ecological functions. Comparing the scaling relationships of wings and hindlimbs highlights how locomotor costs influence the scaling of limb inertial properties. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 14–31.     

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission (“sensory drive”) or because morphological adaptation to different foraging niches causes divergence in “magic traits” associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.