Migratory birds that breed at high latitudes and winter in regions close to and beyond the equator face two particular problems in the control of their annual cycles. First, birds that winter near the equator can spend half of each year under constant daylengths. Hence, in contrast to other species, such birds cannot rely on changes in daylength for timing those seasonal activities that occur in their wintering areas, notably the spring departure for breeding areas. Moreover, in many of these regions, other environmental factors also vary little or unpredictably through the year, and so are unreliable as seasonal cues. Second, unlike birds that remain at mid to high latitudes year round, long-distance migrants that cross the equator are exposed to relatively long days in both summer and 'winter' (= austral summer). They breed during the long days of the boreal summer, but not in those of the austral summer, even though conditions in their austral 'wintering' areas may be similar to those that stimulate reproduction in their northern breeding areas. These facts raise questions in such long-distance migrants: what prevents reproduction in wintering areas, yet stimulates pre-nuptial moult, migratory fattening and departure at appropriate dates? Again, the evidence suggests the intervention of an endogenous time-keeper.
In resident birds of higher latitudes, present in the same locality year-round, control of the annual cycle by an endogenous rhythm, kept to time by daylength changes, would seem relatively straightforward, because at any one locality, day-length varies in a consistent fashion from year to year, providing a reliable indication of date. In fact, in this situation an endogenous rhythm seems unnecessary. In long-distance migrants, however, the situation is more complicated because within the space of a few days birds can pass rapidly from one daylength regime to another. The most obvious way to cope with such problems is to restrict the period of response to daylength to only part of the year, using that period for 'clock-setting', and then allowing the internal rhythm to run for a period, regardless of external daylength. The existence of a 'refractory period', when birds do not respond by gonad growth to otherwise stimulatory daylengths, is consistent with such a mechanism, as is the finding above, that long-distance migrants (exposed to the most rapid and complex changes in daylength regime) rely more heavily on a self-sustaining internal rhythm than do short-distance migrants and residents (Gwinner 1972). The critical photoperiod for the ending of photo-refractoriness, which prevents the gonads of migrants from developing in the austral summer, is related to the photoperiodic conditions of the 'wintering' areas (Gwinner & Helm 2003).
Not surprisingly, endogenous factors seem to have more influence on the timing of migration in species that migrate to the tropics and beyond, and winter far from their breeding areas, than in species that migrate short distances within the northern continents (Gwinner 1972, Hagan et al. 1991). Thus, the long-distance migratory Willow Warblers Phylloscopus trochilus that winter in the tropics, displayed in experimental conditions a firm endogenous control of migratory restlessness, with changes in body weight and moult persisting for more than two years in a constant 12-hour photoperiod (L12:D12). In contrast, closely related but short-distance migratory Chiffchaffs P. collybita, that winter in temperate and Mediterranean zones, lost any endogenous control of these activities within a year, so that body weight became almost constant, and migratory restlessness and moult became irregular or ceased (Gwinner 1971, 1972). Kept under natural daylengths, Willow Warblers moulted earlier and more rapidly than Chiffchaffs; they prepared for migration earlier, and showed more fattening and restlessness. Most of these differences persisted when birds were kept under constant daylengths, indicating some degree of endogenous control. The same was found for different races of Stonechats Saxicola torquata kept in the same, constant conditions (Gwinner & Helm 2003).
It seems, then, that in long-distance migrants that winter in the tropics and beyond, endogenous time programmes may operate for the entire life of the individual, and regulate the timing of all seasonal activities, whether reproduction, moult, fat deposition or migratory restlessness. Although the cycles do not require environmental cues to operate, but are intrinsic to the individual, they are normally synchronised by changes in daylength that keep the endogenous components in step with the seasons. Evidence of genetic influence on annual cycles derives partly from the fact that, on natural daylengths, first-generation hybrids have shown patterns of migratory timing and fat deposition that are intermediate between those of their parents (for waterfowl see Murton & Westwood 1977, for Sylvia warblers see Berthold 1984, 1990, for Phoenicurus redstarts see Berthold 1990, for Stonechats Saxicola torquata see Helm & Gwinner 1999). Other evidence of genetic influence comes from heritability studies based on parent-offspring comparisons (for breeding dates see van Noordwijk et al. 1981; for moult see Larsson 1996; for migration dates see M0ller 2001, Pulido et al. 2001, Pulido & Berthold 2003, Chapter 20). Still further evidence comes from the changes that have occurred in wild birds in response to particular selection pressures (for laying dates of Great Tit Parus major see Visser et al. 1998, for spring migration dates of Cliff Swallow Petrochelidon pyrrhonota see Brown & Brown 2000).
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