Fuel Deposition Of Shorebirds At Stopping Sites In The Yellow Sea During Spring Migration

Migratory birds require one or more stopping sites to rest or to refuel during long-distance flights. Habitat loss and degradation at stopping sites are the main threats to migratory shorebirds. Bird surveys in the last two decades have highlighted the importance of the tidal wetlands in the Yellow Sea for migratory shorebirds, with over three million shorebirds staying in the Yellow Sea during spring and autumn migration. However, the functions of different stopping sites within this area for fuel deposition of migratory shorebirds remain unclear. Using bird counts, body composition analysis, flight model simulation, radio-tracking study, orientation cage experiment, and plasma metabolite analysis, I studied fuel deposition of shorebirds at different stopping sites in the Yellow Sea during spring migration, in respect of their physiology, behavior and ecology. This study focused on the three shorebird species:the red knot(Calidris canutus), the great knot (Calidris tenuirostris) and the red-necked stint (Calidris ruficollis). The study area included Chongming Dongtan in the south Yellow Sea, and Nanpu tideland and the Yalu Estuary in the north Yellow Sea. The main conclusions of this study are listed as follows.1) Previous studies indicate there are two phases in the refueling of the long-distance migratory birds at stopping sites:they mainly deposit protein in the first phase and fat in the second phase. Moreover, organs unrelated to the flight, such as nutrient organs, shrink before long-distance non-stop flight to decrease body mass and energy consumption during flight. The current study indicated that at the final refueling site before flying to the breeding grounds (the north Yellow Sea), the fuel deposition pattern of three shorebird species was different from the two-phase pattern. The piersmai red knots showed a three-phase refueling pattern:along with the body mass increase, they first deposit protein in the first phase, then mainly fat in the second phase, and protein again in the last phase. The great knots replenished protein in a similar three-phase way as the red knot, and they deposited fat with a two-phase pattern:little in the first phase and substantially in the second phase. The red-necked stints accumulated protein little at the first and substantially later during staging, and they deposited fat constantly when the body mass increased. All three species did not shrink their nutrient organs before migratory departure. The refueling patterns and phenotypic changes in the current study might be related to the energetic and temporal pressure which long-distance migratory shorebirds experience at their breeding grounds. Accumulating large amounts of protein rapidly in the late period of refueling could decrease the costs of self-maintenance at stopping sites; maintaining the nutrient organs could help bringing extra energy and nutrients to the breeding grounds and save the cost of rebuilding the organs at the destination. The result of the current study might be an evidence of carry-over effects between different life history stages of migratory birds. Selection pressure from the next stage could also possibly influence the physiological and ecological performance in the current stage.2) The migration period of all four shorebird species (subspecies) was almost or more than one month in both the south and the north Yellow Sea, and there was an overlap between migration periods of the same species at the two sites. In species with "jumping" and "hopping" strategy, the overlap respectively took about 70% and 38% of their migration period in the south Yellow Sea. In the south Yellow Sea, the daily mean body mass of all four species (subspecies) did not increase significantly or increased slowly with the date. They deposited little fuel and could not fly to the breeding grounds directly. In the north Yellow Sea, however, the daily mean body mass of shorebirds increased rapidly with the date. The birds deposited large amounts of fuel and were able to fly non-stop to the breeding grounds. The individual length of stay of great knots was 2.3±1.9 d (n=40) in the south, and 31.0 ±13.6 d (n=22) in the north. The results of the current study indicate that different stopping sites in the south and north Yellow Sea have different functions for shorebird migration in spring. The north Yellow Sea is an important refueling site; and the south Yellow Sea is a temporary resting site for the jumpers, but is especially important for weak individuals and under adverse weather conditions. The jumpers could skip stopping sites in the south and directly arrive at the north Yellow Sea, while the hoppers required to stay at both sites.3) In the south Yellow Sea, the great knots showed stronger migratory restlessness with more wind assistance. This was in accordance with their tendency to depart in tailwind and to stay in headwind in the field, indicating that the migration of shorebirds might mainly be affected by exogenous factors (such as wind) in the south Yellow Sea. In the north Yellow Sea, the great knot restlessness increased with the date, while the body mass and wind effect had no positive influence on their restlessness. Bird surveys and radio-tracking studies indicated that most great knots departed from the north Yellow Sea within one week in late May. These results suggested that migratory departure of shorebirds in the north Yellow Sea might be strongly affected by endogenous factors. The direction preference of great knots in the orientation cages did not correspond to the migration direction, but was facing into the ground wind, indicating they preferred taking-off against the wind. The migratory restlessness and orientation behavior of the great knots were not affected by their fuel deposition. This study suggests that shorebird migration might be regulated by different factors in the south and the north Yellow Sea.4) The plasma triglyceride concentration of great knots was higher and plasma β-hydroxybutyrate concentration was lower in the north than in the south Yellow Sea. This indicates birds have higher refueling rate in the north than in the south stopping sites. Moreover, the ratio of plasma triglyceride and phospholipid concentration was higher in the north than in the south, suggesting the food quality might be better in the north Yellow Sea, and this might be related to the spatial difference in great knot refueling rate. The results of the current study prove that the north Yellow Sea is an important refueling site, and indicate high-quality food resources in this area benefit the fuel deposition of shorebirds.In summary, the stopping sites in the south and the north Yellow Sea have different functions for shorebird fuel deposition during migration. The south Yellow Sea is a temporary resting site. Shorebird individuals stay in the south Yellow sea for a short period and deposit little fuel with low refueling rate. Their migration is affected mainly by the exogenous factors. Therefore the south Yellow Sea is especially important for weak individuals and under adverse weather conditions. In contrast, the north Yellow Sea is an important refueling site. Shorebird individuals stay in the north Yellow Sea for a long period and deposit large amounts of fuel with high refueling rate. Their migration is mainly affected by endogenous factors. Moreover, the physiology and behavior of shorebirds in the north Yellow Sea, their final stopping site before flying to the breeding grounds, reflect the selection pressure not only enroute, but also from the breeding grounds, suggesting an intimate connection between different stages of the life history.