The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration

The small size of the billions of migrating songbirds commuting between temperate breeding sites and the tropics has long prevented the study of the largest part of their annual cycle outside the breeding grounds. Using light-level loggers (geolocators), we recorded the entire annual migratory cycle of the red-backed shrike Lanius collurio, a trans-equatorial Eurasian-African passerine migrant. We tested differences between autumn and spring migration for nine individuals. Duration of migration between breeding and winter sites was significantly longer in autumn (average 96 days) when compared with spring (63 days). This difference was explained by much longer staging periods during autumn (71 days) than spring (9 days). Between staging periods, the birds travelled faster during autumn (356 km d(-1)) than during spring (233 km d(-1)). All birds made a protracted stop (53 days) in Sahelian sub-Sahara on southbound migration. The birds performed a distinct loop migration (22 000 km) where spring distance, including a detour across the Arabian Peninsula, exceeded the autumn distance by 22 per cent. Geographical scatter between routes was particularly narrow in spring, with navigational convergence towards the crossing point from Africa to the Arabian Peninsula. Temporal variation between individuals was relatively constant, while different individuals tended to be consistently early or late at different departure/arrival occasions during the annual cycle. These results demonstrate the existence of fundamentally different spatio-temporal migration strategies used by the birds during autumn and spring migration, and that songbirds may rely on distinct staging areas for completion of their annual cycle, suggesting more sophisticated endogenous control mechanisms than merely clock-and-compass guidance among terrestrial solitary migrants. After a century with metal-ringing, year-round tracking of long-distance migratory songbirds promises further insights into bird migration.     

Weak migratory connectivity,loop migration and multiple non-breeding site use in British breeding Whinchats Saxicola rubetra

Determining the links between breeding populations and the pressures, threats and conditions they experience presents a challenge for the conservation of migratory birds which can use multiple sites separated by hundreds to thousands of kilometres. Furthermore, migratory connectivity – the connections made by migrating individuals between networks of breeding and non-breeding sites – has important implications for population dynamics. The Whinchat Saxicola rubetra is declining across its range, and tracking data from a single African non-breeding site implies high migratory spread. We used geolocators to describe the migration routes and non-breeding areas of 20 Whinchats from three British breeding populations. As expected, migratory spread was high, with birds from the three populations overlapping across a wide area of West Africa. On average, in non-breeding areas, British breeding Whinchats were located 652 km apart from one another, with some likely to share non-breeding areas with individuals from breeding populations as far east as Russia. Four males made a direct non-breeding season movement to a second, more westerly, non-breeding location in January. Autumn migration was through Iberia and around the western edge of the Sahara Desert, whereas spring migration was more direct, indicating an anticlockwise loop migration. Weak migratory connectivity implies that Whinchat populations are somewhat buffered against local changes in non-breeding conditions. If non-breeding season processes have played a role in the species’ decline, then large-scale drivers are likely to be the cause, although processes operating on migration, or interactions between breeding and non-breeding processes, cannot be ruled out.     

Climatic connectivity between Africa and Europe may serve as a basis for phenotypic adjustment of migration schedules of trans-Saharan migratory birds

Most European migratory birds wintering in sub‐Saharan Africa have anticipated arrival to the breeding areas over the past decades. This phenological change may be ultimately caused by warming of the Northern Hemisphere via evolutionary changes or phenotypic plasticity in migration behavior. First arrival dates are negatively predicted by temperatures upon arrival to the breeding grounds. This seems puzzling, because migrants should be unable to predict weather conditions at long range. Migrants can enjoy diverse fitness benefits from early arriving. However, if weather conditions at destination cannot be predicted, early arrival can also entail severe costs. If meteorological conditions in Europe during breeding covary with those in sub‐Saharan Africa during late winter, long‐distance migrants may have a clue to predict meteorological conditions in their breeding areas while they are still in Africa and adjust their migration schedule consequently, an idea that has never been tested. We analyzed the correlation between March–April temperature anomalies (T_an) in Europe and February T_an in the Sahel and sub‐Sahel, where long‐distance migrants winter or stop‐over. T_an in Africa negatively predicted T_an in Europe, the association being particularly strong (unsigned effect size, z_r>0.35) for eastern Sahel and northern and eastern Europe, where the risks of early arrival may be larger. However, the strength of the correlations between T_an in the two continents has declined during the last 25 years; thus, possibly, partly compromising adaptive mechanisms of adjustment of migration. The existence of such climatic connectivity leads to several predictions, including that positive T_an in Africa should delay arrival. Consistent with this prediction, we found that first arrival dates of seven long‐distance migratory species positively covaried with February T_an in Africa. Thus, while wintering, migrants might be able to predict meteorological conditions at the beginning of the breeding season, and phenotypically adjust migration schedules to optimally tune arrival date.     

Flexibility in the timing of post‐breeding moult in passerines in the UK

Higher temperatures resulting from climate change have led to predictions that the duration of the breeding season of many temperate bird species may be changing. However, the extent to which breeding seasons can be altered will also depend on the degree of flexibility in processes occurring at other points in the annual cycle. In particular, plasticity in the timing of post‐breeding moult (PBM) could facilitate changes in the timing of key events throughout the annual cycle, but little is known about the level of within‐ and between‐species plasticity in PBM. As part of the British Trust for Ornithology (BTO) Ringing Scheme, many ringers routinely record moult scores of flight feathers, and these can be used to provide information on the annual progression of PBM for a range of species. Here we use ringing data to investigate patterns of PBM in 15 passerines, as well as data from the BTO Nest Record Scheme to relate these differences to the timing of breeding of these species across the UK. We find considerable variation in both the mean start (19 May–29 July) and duration (66–111 days) of PBM between species, but find no evidence that species starting PBM later in the season complete it any faster. However, there is considerable within‐species variation in PBM, particularly for multi‐brooded species; PBM starts later and is completed in less time when the duration of the breeding season (difference between first and last nests) is longer. This implies that a later end to breeding can be compensated for by faster PBM, and that advances in breeding could lead to earlier and slower PBM. Our findings suggest that adaptation of PBM in response to climate‐mediated changes in the timing and duration of the breeding season is possible. However, the requirement to complete PBM prior to migration or the onset of winter might constrain the extent to which breeding seasons can lengthen, especially for later nesting species.     

Patterns in departure phenology and mass gain on African non‐breeding territories prior to the Sahara crossing in a long‐distance migrant

Afro‐Palaearctic migrants are declining to a greater degree than other European species, suggesting that processes occurring in Africa or on migration may be driving these trends. Constraints on food availability on the wintering grounds may contribute to these declines but little is known about when and where these resource constraints may occur. Sufficient resources are particularly important prior to spring migration, when migrants must cross the Sahara Desert. We examined mass gain and departure phenology in a long‐distance Palaearctic passerine migrant to determine the degree to which pre‐migratory fattening occurs in their long‐term non‐breeding territories in the Guinea Savannah region of Africa. We monitored 75 Whinchats Saxicola rubetra for departure from their non‐breeding territories in one spring, and analysed mass data of 377 Whinchats collected over three non‐breeding seasons plus 141 migrating Whinchats caught in April over 8 years, all within the same few square kilometres of human‐modified Guinea Savannah in central Nigeria. Whinchats left their winter territories throughout April, with males departing on average 8 days earlier than females. However, there was no evidence that time of departure from territory was linked to age, body size or mass at capture. Whinchats departed their territories with a predicted mass of 16.8 ± 0.3 g, considerably less than the c. 24 g required for the average Whinchat to cross the Sahara directly. Comparing departure dates with arrival dates in southern Europe showed a discrepancy of at least 2 weeks, suggesting that many Whinchats spend considerable time on pre‐migratory fuelling outside their winter territory prior to crossing the Sahara. Overwintering birds gained mass slowly during February and March (0.03 g/day), and non‐territorial or migrating birds at a much higher rate in April (at least 0.23 g/day), with up to 20% of migrating Whinchats in April potentially having sufficient fuel loads to cross the Sahara directly from central Nigeria. Our results suggest that most Whinchats leave their winter territories to fatten up locally or, possibly, by staging further north, closer to the southern limit of the Sahara. Resource constraints are therefore likely to be particularly focused in West Africa during mid‐April and possibly at staging areas before the crossing of the Sahara Desert.     

Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability

This paper reviews information from ecological and physiological studies to assess how extrinsic factors can modulate intrinsic physiological processes. The annual cycle of birds is made up of a sequence of life-history stages: breeding, moult and migration. Each stage has evolved to occur at the optimum time and to last for the whole duration of time available. Some species have predictable breeding seasons, others are more flexible and some breed opportunistically in response to unpredictable food availability. Photoperiod is the principal environmental cue used to time each stage, allowing birds to adapt their physiology in advance of predictable environmental changes. Physiological (neuroendocrine and endocrine) plasticity allows non-photoperiodic cues to modulate timing to enable individuals to cope with, and benefit from, short-term environmental variability. Although the timing and duration of the period of full gonadal maturation is principally controlled by photoperiod, non-photoperiodic cues, such as temperature, rainfall or food availability, could potentially modulate the exact time of breeding either by fine-tuning the time of egg-laying within the period of full gonadal maturity or, more fundamentally, by modulating gonadal maturation and/or regression. The timing of gonadal regression affects the time of the start of moult, which in turn may affect the duration of the moult. There are many areas of uncertainty. Future integrated studies are required to assess the scope for flexibility in life-history strategies as this will have a critical bearing on whether birds can adapt sufficiently rapidly to anthropogenic environmental changes, in particular climate change.     

Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird

We studied variation in arrival date to the breeding colonies in Italy of a trans‐Saharan migratory bird, the barn swallow Hirundo rustica, in relation to variation in ecological conditions, as reflected by the normalized difference vegetation index (NDVI), in the winter quarters. Arrival date of old but not young individuals captured during consecutive breeding seasons was earlier after winters with favourable conditions. Change in arrival date in relation to change in NDVI was similar in the two sexes. Change in arrival date significantly and positively predicted change in breeding date. As a result of increased frequency of second broods determined by earlier arrival, the number of fledged offspring per season was larger after African winters with good in comparison to poor ecological conditions for barn swallows. This is the first study demonstrating phenotypic plasticity in migration phenology of a long‐distance migratory bird in relation to ecological conditions during wintering.     

The cost of migration: spoonbills suffer higher mortality during trans-Saharan spring migrations only

Explanations for the wide variety of seasonal migration patterns of animals all carry the assumption that migration is costly and that this cost increases with migration distance. Although in some studies, the relationships between migration distance and breeding success or annual survival are established, none has investigated whether mortality during the actual migration increases with migration distance. Here, we compared seasonal survival between Eurasian spoonbills (Platalea leucorodia leucorodia) that breed in The Netherlands and migrate different distances (ca 1000, 2000 and 4500 km) to winter in France, Iberia and Mauritania, respectively. On the basis of resightings of individually marked birds throughout the year between 2005 and 2012, we show that summer, autumn and winter survival were very high and independent of migration distance, whereas mortality during spring migration was much higher (18%) for the birds that wintered in Mauritania, compared with those flying only as far as France (5%) or Iberia (6%). As such, this study is the first to show empirical evidence for increased mortality during some long migrations, likely driven by the presence of a physical barrier (the Sahara desert) in combination with suboptimal fuelling and unfavourable weather conditions en route.     

Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants

Long-distance migration, and the study of the migrants who undertake these journeys, has fascinated generations of biologists. However, many aspects of the annual cycles of these migrants remain a mystery as do many of the driving forces behind the evolution and maintenance of the migrations themselves. In this article we discuss nutritional, energetic, temporal and disease-risk bottlenecks in the annual cycle of long-distance migrants, taking a sandpiper, the red knot Calidris canutus, as a focal species. Red knots have six recognized subspecies each with different migratory routes, well-known patterns of connectivity and contrasting annual cycles. The diversity of red knot annual cycles allows us to discuss the existence and the effects of bottlenecks in a comparative framework. We examine the evidence for bottlenecks focusing on the quality of breeding plumage and the timing of moult as indicators in the six subspecies. In terms of breeding plumage coloration, quality and timing of prealternate body moult (from non-breeding into breeding plumage), the longest migrating knot subspecies, Calidris canutus rogersi and Calidris canutus rufa, show the greatest impact of bottlenecking. The same is true in terms of prebasic body moult (from breeding into non-breeding plumage) which in case of both C. c. rogersi and C. c. rufa overlaps with southward migration and may even commence in the breeding grounds. To close our discussion of bottlenecks in long-distance migrants, we make predictions about how migrants might be impacted via physiological 'trade-offs' throughout the annual cycle, using investment in immune function as an example. We also predict how bottlenecks may affect the distribution of mortality throughout the annual cycle. We hope that this framework will be applicable to other species and types of migrants, thus expanding the comparative database for the future evaluation of seasonal selection pressures and the evolution of annual cycles in long-distance migrants. Furthermore, we hope that this synthesis of recent advancements in the knowledge of red knot annual cycles will prove useful in the ongoing attempts to model annual cycles in migratory birds.     

Does climate change explain the decline of a trans-Saharan Afro-Palaearctic migrant?

There is an urgent need to understand how climate change will impact on demographic parameters of vulnerable species. Migrants are regarded as particularly vulnerable to climate change; phenological mismatch has resulted in the local decline of one passerine, whilst variations in the survival of others have been related to African weather conditions. However, there have been few demographic studies on trans-Saharan non-passerine migrants, despite these showing stronger declines across Europe than passerines. We therefore analyse the effects of climate on the survival and productivity of common sandpipers Actitis hypoleucos, a declining non-passerine long-distant migrant using 28 years’ data from the Peak District, England. Adult survival rates were significantly negatively correlated with winter North Atlantic Oscillation (NAO), being lower when winters were warm and wet in western Europe and cool and dry in northwest Africa. Annual variation in the productivity of the population was positively correlated with June temperature, but not with an index of phenological mismatch. The 59% population decline appears largely to have been driven by reductions in adult survival, with local productivity poorly correlated with subsequent population change, suggesting a low degree of natal philopatry. Winter NAO was not significantly correlated with adult survival rates in a second, Scottish Borders population, studied for 12 years. Variation in climatic conditions alone does not therefore appear to be responsible for common sandpiper declines. Unlike some passerine migrants, there was no evidence for climate-driven reductions in productivity, although the apparent importance of immigration in determining local recruitment complicates the assessment of productivity effects. We suggest that further studies to diagnose common sandpiper declines should focus on changes in the condition of migratory stop-over or wintering locations. Where possible, these analyses should be repeated for other declining migrants.     

Evidence of postbreeding prospecting in a long‐distance migrant

1. Organisms assess biotic and abiotic cues at multiple sites when deciding where to settle. However, due to temporal constraints on this prospecting, the suitability of available habitat may be difficult for an individual to assess when cues are most reliable, or at the time they are making settlement decisions. For migratory birds, the postbreeding season may be the optimal time to prospect and inform settlement decisions for future breeding seasons.
2. We investigated the fall movements of flammulated owls (Psiloscops flammeolus) within breeding habitat after fledglings had gained independence and before adults left for migration. From 2013 to 2016, we trapped owls within a breeding population wherein all nesting owls and their young have been banded since 1981. We used stable isotopes in combination with mark–recapture data to identify local individuals and differentiate potential prospecting behavior from other seasonal movements such as migration or staging.
3. We commonly captured owls in the fall—predominantly hatch‐year owls—that were not known residents of the study area. Several of these nonresident owls were later found breeding within the study area. Stable isotope data suggested a local origin for virtually all owls captured during the fall.
4. Our results suggest that hatch‐year flammulated owls, but also some after‐hatch‐year owls, use the period between the breeding season and fall migration to prospect for future breeding sites. The timing of this behavior is likely driven by seasonally variable costs associated with prospecting.
5. Determining the timing of prospecting and the specific cues that are being assessed will be important in helping predict the extent to which climate change and/or altered disturbance regimes will modify the ecology, behavior, and demographics associated with prospecting.

     

The grand challenges of migration ecology that radar aeroecology can help answer

Many migratory species have experienced substantial declines that resulted from rapid and massive expansions of human structures and activities, habitat alterations and climate change. Migrants are also recognized as an integral component of biodiversity and provide a multitude of services and disservices that are relevant to human agriculture, economy and health. The plethora of recently published studies reflects the need for better fundamental knowledge on migrations and for better management of their ecological and human‐relevant effects. Yet, where are we in providing answers to fundamental questions and societal challenges? Engaging a broad network of researchers worldwide, we used a horizon‐scan approach to identify the most important challenges which need to be overcome in order to gain a fuller understanding of migration ecology, and which could be addressed using radar aeroecological and macroecological approaches. The top challenges include both long‐standing and novel topics, ranging from fundamental information on migration routes and phenology, orientation and navigation strategies, and the multitude of effects migrants may have on resident communities, to societal challenges, such as protecting or preventing migrant services and disservices, and the conservation of migrants in the face of environmental changes. We outline these challenges, identify the urgency of addressing them and the primary stakeholders – researchers, policy makers and practitioners, or funders of research.     

Breeding status influences timing but not duration of moult in the Northern Fulmar Fulmarus glacialis

Seabirds are key marine top predator species that are often used as indicators of the environmental quality of the oceans. Their breeding phenology has been studied extensively, but their pelagic habits mean less is known about the phenology of other events during the non-breeding period. Here, we used miniaturized saltwater immersion light-based geolocators (GLS) to investigate moult phenology in individuals with known breeding histories in a population of Northern Fulmar Fulmarus glacialis in Orkney, Scotland. As seabirds spend more time on the water during moult, moulting periods can be identified from patterns of variation in the amount of time that birds are in contact with saltwater. Estimates of daily variation in this behaviour during the non-breeding period were based upon wet/dry sensors and then modelled to characterize the timing of the moult. Light-based geolocation provided information on the areas used by each individual during its moult period. Inter-individual variability in moult timing was investigated in relation to sex and breeding success in the previous summer. We found a sex difference in the location of the moult, but not in its timing. However, the timing of moult did differ between individuals that had succeeded or failed in their previous breeding attempt, with successful breeders moulting the latest. In contrast, the duration of moult did not depend on prior reproductive success, but there was evidence of inter-annual variation in moult duration. GLS studies have provided a step change in our understanding of the at-sea distribution of pelagic seabirds. Our work highlights how activity data from these devices can add value to such studies by identifying key phases of the annual cycle, and locations at these times, when seabirds may be at particular risk. Furthermore, our findings indicate that individual and inter-annual variation in breeding success may influence phenological patterns in other phases of the Northern Fulmar annual cycle.     

Cavity use throughout the annual cycle of a migratory woodpecker revealed by geolocators

The importance of cavities as roost sites in migratory species is often unknown because it is challenging to monitor cavity use during the non‐breeding period. We documented cavity use throughout the annual cycle of a woodpecker using light‐level geolocators. Northern Flickers Colaptes auratus spent 63–90% of nights roosting in a cavity throughout the year, including during migration. The high frequency of year‐round cavity use by Flickers suggests that cavities provide benefits beyond nest‐sites. Our work highlights the potential use of geolocators to examine cavity use.     

The relationship of the phase and amplitude of the annual cycle of CO2 to phenological events

Background: A key current issue in studies of global CO₂ is the cause of the recent pronounced changes in the timing (phase) and amplitude of its annual cycle.

Aim: To use a sensitivity analysis in order to identify the most influential parameters in a new four-box diffusion model of global CO₂ transport.

Methods: A new diffusion model of global atmospheric transport is developed, implemented by optimisation and used to assess the effects of oceanic, terrestrial and anthropogenic CO₂ fluxes on the annual CO₂ cycle. As the terrestrial phenology of living organisms in the temperate zones is identified as the central process of concern an improved phenological model for the temperate zones is proposed and used in up-scaling from plant to planet.

Results: The diffusion model is found to be able to mimic many of the features observed by the GLOBALVIEW-CO₂ network, including the global trend, latitudinal gradient, and annual waveform.

Conclusions: It is concluded that, out of five rival hypotheses considered at the outset, the springtime phenology of terrestrial biomes is the dominant controller of recent changes to the annual CO₂ cycle.     

Canopy duration has little influence on annual carbon storage in the deciduous broad leaf forest

Vegetation phenology, the study of the timing and length of the terrestrial growing season and its connection to climate, is increasingly important in integrated Earth system science. Phenological variability is an excellent barometer of short‐ and long‐term climatic variability, strongly influences surface meteorology, and may influence the carbon cycle. Here, using the 1895–1993 Vegetation/Ecosystem Modelling and Analysis dataset and the Biome‐BGC terrestrial ecosystem model, we investigated the relationship between phenological metrics and annual net ecosystem exchange (NEE) of carbon. For the 1167 deciduous broad leaf forest pixels, we found that NEE was extremely weakly related to canopy duration (days from leaf appearance to complete leaf fall). Longer canopy duration, did, however, sequester more carbon if warm season precipitation was above average. Carbon uptake period (number of days with net CO₂ uptake from the atmosphere), which integrates the influence of all ecosystem states and processes, was strongly related to NEE. Results from the Harvard Forest eddy‐covariance site supported our findings. Such dramatically different results from two definitions of ‘growing season length’ highlight the potential for confusion among the many disciplines engaged in phenological research.     

Climate change and the optimal flowering time of annual plants in seasonal environments

Long‐term phenology monitoring has documented numerous examples of changing flowering dates during the last century. A pivotal question is whether these phenological responses are adaptive or not under directionally changing climatic conditions. We use a classic dynamic growth model for annual plants, based on optimal control theory, to find the fitness‐maximizing flowering time, defined as the switching time from vegetative to reproductive growth. In a typical scenario of global warming, with advanced growing season and increased productivity, optimal flowering time advances less than the start of the growing season. Interestingly, increased temporal spread in production over the season may either advance or delay the optimal flowering time depending on overall productivity or season length. We identify situations where large phenological changes are necessary for flowering time to remain optimal. Such changes also indicate changed selection pressures. In other situations, the model predicts advanced phenology on a calendar scale, but no selection for early flowering in relation to the start of the season. We also show that the optimum is more sensitive to increased productivity when productivity is low than when productivity is high. All our results are derived using a general, graphical method to calculate the optimal flowering time applicable for a large range of shapes of the seasonal production curve. The model can thus explain apparent maladaptation in phenological responses in a multitude of scenarios of climate change. We conclude that taking energy allocation trade‐offs and appropriate time scales into account is critical when interpreting phenological patterns.