Rapid Advance of Spring Arrival Dates in Long-Distance Migratory Birds

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Science  30 Jun 2006:
Vol. 312, Issue 5782, pp. 1959-1961
DOI: 10.1126/science.1126119


Several bird species have advanced the timing of their spring migration in response to recent climate change. European short-distance migrants, wintering in temperate areas, have been assumed to be more affected by change in the European climate than long-distance migrants wintering in the tropics. However, we show that long-distance migrants have advanced their spring arrival in Scandinavia more than short-distance migrants. By analyzing a long-term data set from southern Italy, we show that long-distance migrants also pass through the Mediterranean region earlier. We argue that this may reflect a climate-driven evolutionary change in the timing of spring migration.

Many biological processes are affected by climate, and in temperate areas the increasing spring temperature over the past 20 to 30 years has caused an advancement of phenological events in plants and invertebrates (1, 2). The earlier onset of spring has consequences for the timing of breeding in birds, which has evolved to match peak food availability (3, 4). We may therefore expect the timing of breeding to track any temporal shift in food availability caused by a trend in spring temperature (5). Most passerine birds breeding in temperate areas of the Northern Hemisphere are seasonal migrants, and the timing of migration ultimately constrains when breeding can start (6, 7). Short-distance migrants, spending the winter close to the breeding grounds, may be able to adjust the timing of migration in response to local climate change, which will be correlated to the conditions on the breeding grounds. In tropical-wintering long-distance migrants, the timing of migration is under endogenous control (8, 9), and the cues needed to trigger the onset of migration are unlikely to be linked to the climate on their breeding grounds. Therefore, it has been assumed that short-distance migrants are more likely than long-distance migrants to vary migration timing in response to climate change (10). Here we show that such an assumption is not empirically justified.

We estimated trends in arrival time for the early, middle, and late phases of migration (that is, the species- and site-specific 10th, 50th, and 90th percentiles of the spring arrival distribution) in short- and long-distance passerine migrants, based on long-term banding and observational data (from 1980 to 2004) from four bird observatories in Scandinavia and a site in southern Italy (11, Fig. 1). We also investigated whether year-to-year variation in arrival time can be explained by short-term climate variability as measured by the North Atlantic Oscillation (NAO) (12). As explanatory variables we used the calendar year (TIME) and the deviations from linear regression of the winter NAO index on year [dNAO; the trend in NAO was weakly negative over this time period (11)]. Spring migration might advance for two distinct reasons. First, there can be a microevolutionary (genetic) response to the selection pressures for earlier breeding. Second, the migrants can show a phenotypically plastic response to trends in weather or climatic patterns on the wintering ground and/or along the migration route, whereby if spring arrives early on the wintering grounds, spring migration will also start early. Thus, a response to TIME may reflect either microevolutionary change or phenotypic plasticity, whereas a response to dNAO indicates exclusively phenotypic plasticity in the migratory behavior.

Fig. 1.

The locations of the four bird observatories (F, Falsterbo, 55°23′N, 12°49′E; O, Ottenby, 56°12′N, 16°24′E; J, Jomfruland, 58°53′N, 9°37′E; H, Hanko, 59°48′N, 22°53′E) and of the banding site on Capri (C, 40°33′N, 14°15′E).

Long-distance migrants have advanced their arrival in northern Europe in all phases of migration (Fig. 2 and tables S1 to S3). The advancement in long-distance migrants is strongest in the early phase of migration, and there is limited variation between species. Furthermore, the analysis of the data set from Italy (from the island of Capri) showed that long-distance migrants wintering south of the Sahara desert are actually arriving in southern Europe progressively earlier. In fact, all of the nine species analyzed show a trend for earlier spring arrival at Capri in most phases of migration (Fig. 2 and table S4). The long-term trend on Capri is at least as strong as that observed in Scandinavia (Fig. 3). In short-distance migrants, instead, we find only a weak trend toward earlier arrival, and there is considerable variation between species (Fig. 2 and tables S1 to S3).

Fig. 2.

Long-term trend (TIME) and the effect of short-term climatic fluctuations (dNAO) on the early [(A), 10th percentile], middle [(B), 50th percentile], and late [(C), 90th percentile] phases of the spring arrival distribution in short-distance migrants (blue circles) and long-distance migrants (red squares) in Scandinavia and on Capri (red triangles). The solid symbols are sample averages, and the ellipses delimit their 95% confidence regions (11). Estimates for each species are given in tables S1 to S4. The differences in effect size for early-phase arrival of short-distance migrants versus long-distance migrants was 0.15 [95% confidence interval (CI): 0.06 to 0.23] days per year for the effect of TIME.

Fig. 3.

Mean slopes and 95% CIs of the relationships between arrival dates and TIME (A to C) or dNAO (D to F) in the early (10th percentile), middle (50th percentile), and late (90th percentile) phases of migration for six species of long-distance migrants for which time series were available at each observatory (solid symbols; F, Falsterbo; O, Ottenby; J, Jomfruland; H, Hanko) and at the banding site on Capri (open symbol; C). The sites are sorted from south to north. Species-specific slopes were estimated with a mixed-effect linear model (11). The correlation between species, when species- and observatory-specific effects of both TIME and dNAO were accounted for, was estimated at 0.48 (95% CI: 0.17 to 0.75), 0.25 (95% CI: 0.04 to 0.51), and 0.34 (95% CI: 0.03 to 0.68) for the 10th, 50th, and 90th percentiles, respectively.

In accordance with previous findings (1315), a high NAO index is associated with the early arrival of short-distance migrants in Scandinavia, but only in the early phase of migration (Fig. 2). On the other hand, most long-distance migrants tend to arrive earlier in Scandinavia during years of high NAO in all phases of migration (Figs. 2 and 3 and tables S1 to S3). The opposite pattern is observed at Capri, where high NAO tends to delay arrival times (Figs. 2 and 3 and data in table S4). The underlying reason for this may be found south of the Sahara desert, because a high NAO index harms productivity over vast areas of northwestern and southeastern Africa (16), which may delay the spring departure of migrants from sub-Saharan wintering areas.

By showing that long-distance migrants have advanced their migration more than short-distance migrants, we have challenged the conventional wisdom that species wintering in temperate Europe should respond more strongly to climate change than trans-Saharan migrants (10). Furthermore, the earlier arrival of trans-Saharan migrants at Capri shows that the temporal trend for earlier arrival in Scandinavia cannot be explained simply by faster migration through Europe in response to a concomitant trend of increasing temperatures taking place within continental Europe (17). Instead it suggests that (i) the onset of migration has advanced, or (ii) the speed of migration through Africa has increased. Both alternatives could be seen as phenotypic responses to trends in the African climate patterns having a positive effect on the foraging conditions (18), thereby improving the birds' physical conditions, which in turn affects their timing of migration (19) and makes the migration (including flight and stopover) more efficient. A positive trend in African temperatures (20) has previously been suggested as a reason why long-distance migrants arrive earlier in northern Europe (21). However, increasing African temperatures should decrease productivity (22), thereby delaying long-distance migrants' departure from the wintering ground. Hence, the earlier arrival is probably not a phenotypic response to improved foraging conditions. More likely, the rapid advance in arrival dates of long-distance migrants in Europe is due to climate-driven evolutionary changes in the timing of spring migration. Even though migratory activity is under endogenous control, experiments have demonstrated individual variation in the response to the photoperiodic cues needed to trigger the mechanisms underlying the onset of migration (23). The passerine birds investigated here reproduce at just 1 year of age and thus have the potential for a rapid evolutionary response to environmental changes. Given the considerable heritable genetic variation in the timing of migration (24, 25) and the selection pressure to breed earlier in Europe (6, 7), a change toward earlier arrival is indeed to be expected.

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Tables S1 to S5


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