Migratory birds track seasonal resources across and between continents. We propose a general strategy of tracking the broad seasonal abundance of resources throughout the annual cycle in the longest-distance migrating land birds as an alternative to tracking a certain climatic niche or shorter-term resource surplus occurring, for example, during spring foliation. Whether and how this is possible for complex annual spatiotemporal schedules is not known. New tracking technology enables unprecedented spatial and temporal mapping of long-distance movement of birds. We show that three Palearctic-African species track vegetation greenness throughout their annual cycle, adjusting the timing and direction of migratory movements with seasonal changes in resource availability over Europe and Africa. Common cuckoos maximize the vegetation greenness, whereas red-backed shrikes and thrush nightingales track seasonal surplus in greenness. Our results demonstrate that the longest-distance migrants move between consecutive staging areas even within the wintering region in Africa to match seasonal variation in regional climate. End-of-century climate projections indicate that optimizing greenness would be possible but that vegetation surplus might be more difficult to track in the future.

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INTRODUCTION

Recently, ethere have been fforts to understand the association between animal movement and the environment have increased. Studies of diverse marine organisms have linked distributions and movements of diverse marine organisms to sea surface temperature and net primary productivity (NPP) (1, 2), whereas elephants track precipitation-driven vegetation dynamics (3) and other ungulates wander to optimize the nutritional content of the grasses they eat (4, 5). Migrating birds also track vegetation dynamics, the so-called green wave surfing; that is, the birds move northward, timed with the seasonally progressing green-up of vegetation (6–8).

The ability to fly makes birds one of the most mobile terrestrial animal groups (9, 10). Long-distance migratory birds commonly explore distantly separated regions between breeding and wintering grounds. They often do so by traveling several thousand kilometers and crossing large inhospitable regions to find areas where environmental conditions can sustain survival (11, 12). In this way, seasonal migration solves the problem of exploiting seasonal resources across the globe (11).

Remote sensing data, such as the satellite-based greenness index NDVI (Normalized Difference Vegetation Index), are increasingly used to infer ecological processes related to movement. Using NDVI, it has been suggested that geese migrating to breeding grounds, at least in some cases, “surf the green wave” of sprouting high-quality grass vegetation (6, 8, 13, 14). Likewise, regional winter movements of Montagu’s harriers (Circus pygargus) have been correlated with decreasing vegetation greenness (15), and bobolinks (Dolichonyx oryzivorus) have been shown to leave grasslands used for stopovers when vegetation conditions deteriorate (16). Moving from breeding grounds in the Northern Hemisphere to wintering grounds in the Southern Hemisphere obviously enables the exploitation of surplus seasonal resources with a clear dynamic link between breeding and wintering resources (17–20). However, the study of the underlying migration pattern drivers throughout more complex annual spatiotemporal schedules has been hampered by the lack of data on the movements of individual birds throughout the year, especially within their tropical wintering area.

Moreau (21) suggested that, in Africa, many migrants follow a strategy of itinerancy, staying in areas only while they are most suitable after seasonal rains. In this way, areas south of the equator become suitable during the austral summer, enabling only the longest-distance migrants, such as thrush nightingales (Luscinia luscinia) and red-backed shrikes (Lanius collurio), to exploit these areas. Inferred from observations of seasonal occurrence, these itinerant schedules have been suggested for thrush nightingales and red-backed shrikes but not for common cuckoos (Cuculus canorus) (22–24).

However, the hypothesized link between movements and seasonal regional resources throughout the annual cycle has never been properly established, and the precise timing of annual individual schedules relative to seasonally induced local dynamics in habitats, food resources, and climate remains restricted to parts of the annual cycle in long-distance migrants (6–8, 13, 15, 16, 25). In order to establish potential links between resources and annual bird movements, we have combined the results of high–temporal resolution tracking of individual birds with monitoring variation in local ecological conditions across the seasonally changing globe. On the basis of these links, we evaluate the potential consequences of end-of-century climate projections.

Overall, birds exploiting seasonal environments need to properly schedule annual events to maximize fitness (26). The optimal timing of events, such as breeding and molting as well as migration, depends on the availability of seasonally changing resources within the annual cycle (27). Resource availability is likely to be most important during breeding; thus, timing of breeding in relation to resource availability will be more important than stopover timing. Arrival well before the peak in insect prey abundance is common in migrants (28, 29), and it may be impossible to consistently maximize local resources throughout the annual cycle.

Food availability is likely to be the most important resource throughout the annual cycle (30, 31), presumably explaining migration to breed at higher latitudes (32) and stopover timing during spring migration (33). Arzel et al. (28) found that breeding coincides with a peak in invertebrate food abundance in migratory ducks but failed to find support for the hypothesis that they would gain a general increase in food abundance by flying north during spring. Other studies have assumed that migrants were either tracking a climatic niche (34) or staying only during a short period with optimal resource availability, mainly limited to the migratory part of the annual cycle (15, 16).

In general, availability of resources such as food is very difficult to estimate, particularly across habitats and climatic zones. We focus on general vegetation measures to estimate food availability on the basis of the well-established principle that food availability is ultimately related to plant productivity (35).

Staying in the greenest vegetation potentially leads to generally high food availability such as that resulting from breeding in the Northern Hemisphere during summer and spending the nonbreeding season in the Southern Hemisphere (36). The accelerating vegetation growth during spring green-up provides another potentially high food availability, also known as surfing the green wave (6, 13), although, for insectivores, the food peak is generally delayed. Avoiding decreasing vegetation conditions could also drive movements (15, 16).

Given the complexities of niche tracking through different climatic zones and the variable demands during breeding and wintering periods, we propose that, instead of following green vegetation conditions or a constant climatic niche, some migrants might use an alternative strategy of more broadly following pulses of resources, that is, high relative availability of local seasonal resources (surplus greenness; see later discussion). Food availability depends not only on productivity but also on the density of consumers sharing the food resource. Resident populations are thought to be limited by food availability during the season when food availability is at its lowest, whereas clutch size is determined by per-capita food availability during the season when food availability is at its highest (37), and seasonality (the difference between minimum and maximum level of resources) has been linked to clutch size (38, 39). Therefore, migrants may potentially be able to exploit excess or surplus resources in seasonal environments where the density of residents is regulated by the productivity in the season where productivity is lowest (40, 41).

We hypothesize that the migrants’ spatiotemporal schedules could maximize greenness, surplus greenness, or change in greenness. We assume that prolonged migration to new staging sites would generally occur based on the expected conditions at the new site rather than on the actual conditions (must be considered unknown to the birds, at the time of movement). Proximate cues presumably only affect local movements [for example, as reported for within-winter movements in a short-distance migrant songbird (42)] because migrants are expected to rely on their innate program to guide them over long distances (43), with this program presumably being adapted to longer-term averages of climate/resource availability. Songbird migrants have been shown to regionally use the same stopover areas for years, irrespective of local conditions (44). Thus, we focus our analyses on average vegetation conditions over a decade to reflect the expected conditions for a migrant.

Newly developed satellite tracking and light level–based geolocation technology now enables us to follow individual, long-distance migratory birds throughout their annual cycles, which permits more direct inferences about the drivers of long-distance migration and regional movements of individuals (45). Using this technology, we followed common cuckoos (n = 8) (46), red-backed shrikes (n = 18) (44, 47), and thrush nightingales (n = 12) (44), between the Palearctic and southern Africa. The migration routes of these three insectivorous species include large parts of Europe and Africa.

We used a satellite-based greenness index, NDVI, to study spatiotemporal dynamics in food availability caused by seasonal variation in sun radiation and rainfall. Local greenness at an intercontinental scale was measured by averaging the observed NDVI between 2000 and 2010 at a biweekly temporal resolution in 2° latitude × 2° longitude squares (absolute greenness; fig. S1). Local biweekly NDVI relative to the annual average (local surplus in greenness; surplus NDVI) was used as a proxy for ephemeral peaks in food resources. Furthermore, we calculated the change in greenness from the previous biweekly period (change NDVI). Migratory animals need to fit their annual schedule to the seasonally available resources (48). We built a simple, coarse-scale simulation framework to investigate whether the observed schedules were optimal with regard to greenness, surplus greenness, or change in greenness compared to an assumption of no optimization (49). The level at which birds select their habitat is not reflected in the available climate data, and favorable conditions could easily exist locally. However, these local conditions could potentially not be driving long-term spatiotemporal schedules. Combined with the large-scale simulation and the similarity in schedules within species, our relatively small sample sizes are likely to reflect each species’ overall resource optimization at the near-global level.

The amount of future suitable nonbreeding habitat is expected to decrease for some sub-Saharan migrants and to increase for others (50). Regardless, suitable areas based on climate change projections will generally be further away from the breeding grounds for trans-Saharan migrants (51). Projections of future climate imply that the spatiotemporal distribution of resources will change, potentially leading to a future mismatch between seasonal resources and birds’ presence (52). We investigated this potential future mismatch by comparing observed migration schedules with end-of-century projections of seasonal vegetation greenness and local surplus of greenness (that is, greenness and surplus greenness, using the decade-wide climatology).