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

Abstract

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.

Figure 1

The global distribution of knots (updated from Piersma & Davidson 1992) highlighting morphological and behavioural congruence as well as genetic structuring in knot flyways. Migratory routes are colour coded to subspecies and grey lines represent routes requiring further study. The South African wintering area present in Piersma & Davidson (1992) is not shown as knots no longer seem to winter there (L. Underhill 2004, personal communication). Shaded areas in the Arctic indicate breeding areas and circles indicate wintering areas. The size of the circle indicates the relative number of birds using the area. Projected above the contemporary distribution of knots is a phenogram summarizing knot population structure (Buehler & Baker 2005) and below a table outlining morphological, migration and population size details: (i) Bill, tarsus and wing length measurements were ranked and averaged for size score, and overall extent of redness and depth of colour were taken into account for rank plumage score (Tomkovich 1992, 2001); (ii) Piersma et al. (2005); (iii) P. F. Battley 2005, personal observation; (iv) T. Piersma & B. Spaans 2005, unpublished data; (v) Baker et al. (2004, 2005a).

Figure 2

A graphical representation of the annual cycles and life-history stages of the knot subspecies. For the life-history stage ‘northward migration’, ‘x’ represents flight and staging, whereas ‘p’ represents pre-migratory mass gain (extrapolated from table 21.1 in Piersma et al. 2005). In all life-history stages, ‘?’ indicates parts of the annual cycle that are not known with certainty. Periods of bottleneck are shown below the life-history stages. In this figure simultaneous prebasic and wing moult is highlighted as an energetic bottleneck, and periods where both moult and migration overlap are represented by lighter grey shading and labelled ‘moult and migration’ in the C. c. rogersi and C. c. rufa subspecies. Periods of the annual cycle in which individuals experience three or more bottlenecks at a time are considered severely bottlenecked. For example, all subspecies are severely bottlenecked during the final stages of northward migration and arrival on the breeding grounds due to the overlap of energetic, temporal and disease-risk bottlenecks.

Figure 3

Trends between breeding plumage and aspects of migration. (a) Breeding plumage coloration, where 6 signifies the darkest colouration (taking into account both overall extent of redness and depth of colour from Tomkovich (1992, 2001), and overall migration distance for a one-way journey (Pearson correlation, 0.751; p=0.043, one tailed). (b) Breeding plumage coloration (as in (a)) and the number of weeks between departure from the moulting area and arrival on the breeding area (Pearson correlation, 0.781; p=0.033, one tailed).