at tropical intertidal sites have lower fueling rates than birds at more southern or ... for time-minimizing migrants, site-average body mass at departure is a ...
T H E U N I S P I E R S M A , DA N N Y I . R O G E R S, PAT R I C I A M . G O N Z Á L E Z , L E O Z WA R T S , L AW R E N C E J . N I L E S , I N Ê S D E L I M A S E R R A N O D O N A S C I M E N T O, C L I V E D. T. M I N T O N , A N D A L L A N J. BA K E R
Fuel Storage Rates before Northward Flights in Red Knots Worldwide Facing the Severest Ecological Constraint in Tropical Intertidal Environments?
R
ED KNOTS ( CALIDRIS CANUTUS) ARE birds of many worlds. These sandpipers breed only on High Arctic tundra but move south from their disjunct, circumpolar breeding areas to nonbreeding sites on the coasts of all continents (apart from Antarctica), between latitudes 58° N and 53° S. Because of their specialized sensory capabilities, Red Knots generally eat hard-shelled prey found on intertidal, mostly soft, substrates. As a consequence, ecologically suitable coastal sites are few and far between, so they must routinely undertake flights of many thousands of kilometers. We present a review of fuel storage rates at 14 staging sites during northward migration, based on published and unpublished data collected in South and North America, Europe and Africa, and Australia and New Zealand. Fuel storage rates are interpreted in relation to latitude and associated ecological factors (climate, food abundance, and prey quality). In contrast to prediction (based on the low costs of living and thus the freedom to allocate nutrients to fuel storage), Red Knots at tropical intertidal sites have lower fueling rates than birds at more southern or northern latitudes. The highest fueling rates occur at the most northerly sites, before the flight to the tundra for breeding. These northern fueling areas offer smaller benthic biodiversity but greater harvestable biomass than circa-tropical sites, at least in spring. Such high biomasses may enable Red Knots to fuel up quickly not only for onward flight, but for survival on an initially food-free tundra as well. As predicted for time-minimizing migrants, site-average body mass at departure is a positive function of fueling rate. Surprisingly, however, departure body mass appears uncorrelated with the estimated length of the ensuing flight. The association between fueling
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Fuel Storage Rates in Red Knots
rates of the highly food- and habitat-specialized Red Knots and latitude provides a first empirical assessment of the intimate interplay between migratory schedules and ecological factors on a world scale.
INTRODUCTION Long-distance migrant birds capitalize on our seasonal world (Alerstam 1990). From a Northern Hemisphere perspective they seem to optimize the use of northern habitats that become available in summer (for breeding) and Southern Hemisphere habitats that offer favorable environmental conditions during the northern winter. Typical landbirds such as passerines tend to use relatively similar habitats during the breeding and the nonbreeding seasons (Rappole 1995); the sandpipers that are the focus of this chapter, however, certainly use habitats in summer that contrast with those they use the rest of the year (Piersma et al. 1996). For breeding they use dry marshlands and tundras, areas that offer protected nesting sites and plentiful food resources for the chicks. During the rest of the year sandpipers use the relatively scarce wetlands of the world, often with a tidal regime, where habitat suitable for nesting is scarce and arthropod food for chicks would be difficult to find. Because potential stopover sites are as scarce as good wintering sites, most sandpiper species must cover the many thousands of kilometers between the southern nonbreeding and the northern breeding grounds in a few longdistance flights (Piersma 1987). Thus, the birds need to store large fuel loads to cover the distances between suitable sites, which in turn requires them to obtain extra energy above the usual requirement for maintaining stable body mass. Fueling rates are arguably the key variable determining the options open to migrant birds (e.g., Alerstam and Lindström 1990; Ens et al. 1994; Alerstam and Hedenström 1998). Daily food intake, and hence fueling rates, may be affected by limited foraging time and/or food availability (Zwarts et al. 1990a; Kvist and Lindström 2000), restricted heat production due to external heat loads in the Tropics (Verboven and Piersma 1995; Battley et al. 2003), organismal design constraints related to the size and capacity of the organ systems (Piersma 2002; Battley and Piersma 2004), predation (van Gils et al. 2004), and quality of the prey (van Gils et al. 2003a). Here we capitalize on the great volume of work done on the worldwide migration system of one of the largest sandpipers, the Red Knot (Calidris canutus [Scolopacidae]) (fig. 21.1), to see whether a comparison between fueling rates at a wide range of coastal sites reveals constraints on daily food intake and fueling rate. For example, in the absence of foraging constraints we would predict fueling rates to be a negative function of other cost factors such as thermoregulation. Thus, fueling rates should be lower where temperatures are lower: the far south and north. Given the limits of current data on the birds, the analysis is restricted to the northward migration. Also, at this point comparative data
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on harvestable food abundance are still too sparse to bring them fully into the analysis (but see Piersma et al. 1993a). With this assessment we aim to provide a solid empirical contribution to the development of “stopover ecology,” the study of the selective forces acting on migrant birds, especially at stopover sites (Lindström 1995). To the best of our knowledge, this is the first presentation and interpretation of fueling rates of a single species at locations worldwide.
STUDY SYSTEM: THE WWW OF RED KNOTS The worldwide web of migration routes spun by Red Knots finds its origin in the circumpolar breeding grounds of this High Arctic breeding species (Piersma et al. 1991, 1996; Harrington 1996; Piersma and Baker 2000). Red Knots breed only on the northernmost lands of the world, often within sight of the Arctic Ocean, where vegetation is usually sparse and environmental conditions even in summer are quite extreme. On the tundra they eat mostly spiders and arthropods, which they obtain by surface pecking (Tulp et al. 1998). Outside the breeding season, Red Knots occur only on coastal sites that offer large expanses of intertidal (preferably soft) substrates, where they feed on hard-shelled prey such as bivalves, gastropods, and sometimes small crustaceans obtained by high-frequency probing (Piersma et al. 1993a, 1993b). Prey is ingested whole and crushed in a strong muscular stomach (Zwarts and Blomert 1992; Piersma et al. 1993c, 1999a). The nonbreeding habitat and diet of Red Knots may relate to their specific sensory capacities (a highly specialized bill-tip organ to find hard objects in soft sediments [Piersma et al. 1995, 1998]) and, perhaps, the peculiarities of their immune system (Piersma 1997, 2003). We interpret the remarkable range in wintering latitudes as reflecting the scarcity, worldwide, of suitable coastal intertidal habitats, that is, habitats rich in high-quality and shallow buried mollusc prey. To optimize intertidal patch use, Red Knots are skilled users of self-collected information on prey abundance (van Gils et al. 2003b) Although Red Knots have a circumpolar breeding distribution, their range is not continuous. Circling the Arctic Ocean, six separate breeding areas host different populations, all of which are now formally recognized as subspecies based on body size and plumage differences (Piersma and Davidson 1992; Tomkovich 2001). From their respective breeding grounds, the different subspecies spread out south to winter in distinct nonbreeding regions. There appears to be little overlap in occurrence between any combination of subspecies except for the temporary overlap of some canutus and islandica subspecies knots in the Wadden Sea, an extensive area of intertidal flats shared by The Netherlands, Germany, and Denmark (Piersma et al. 1995; Nebel et al. 2000), and of roselaari and rufa in Delaware Bay in the eastern United States. Of particular relevance for the comparisons between sites and subspecies made in this chapter is the finding that the extant Red Knots shared a common an-
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Fig. 21.1. Three plates to illustrate the annual cycle and the habitats used by Red Knots. The top photograph shows a flock of nonbreeding Red Knots in gray-colored basic plumage foraging on an intertidal flat in the Dutch Wadden Sea. The middle photograph shows a flock in which many birds have already molted into the rusty-red alternate plumage alighting on a high-tide roost on the on the Banc d’Arguin, Mauritania in April. The bottom photograph shows a flock in mid June, just after arrival on the snow-covered tundra breeding grounds of Taymyr Peninsula, Russia. All photographs by Jan van de Kam.
cestor as recently as within the last 20,000 years or so (Baker et al. 1994; Baker and Marshall 1997). As a result of this recent expansion from a severely bottlenecked stock, the Red Knot subspecies show little genetic divergence across their worldwide range (A. J. Baker and D. M. Buehler, pers. comm.). Just as the geographic occurrence of Red Knots is centered on the Arctic Ocean, the timing of everything that happens during their annual cycle is centered on the brief breeding season in the High Arctic. Red Knots arrive on the tundra as soon as, or even before, the snow begins to melt (Meltofte 1985; Morrison and Davidson 1990; Whitfield and Tomkovich 1996; Tulp et al. 1998). In northeast Canada and northern Greenland the first Red Knots may arrive on the tundra in the last days of May, but on Taymyr Peninsula
in central Siberia, the tundra does not become free from snow until mid-June. The arrival of Red Knots is consequently later (see fig. 21.1). After 1 to 2 weeks of pair formation and territory establishment and 3 weeks of incubation (shared by the partners), the females return to southern coastal nonbreeding areas as soon as the eggs hatch (or the clutch is lost). They are followed almost 4 weeks later by the successful males (who take care of the chicks) and the first fledglings (Whitfield and Brade 1991). By then it is late July and early August, a period with declining arthropod abundances (Schekkerman et al. 2003) and an increasing likelihood of snowfall. Red Knots usually, if not always, migrate in flocks of 10 to 100 birds, usually leaving for long-distance flight in the late afternoon and early evening (Dick et al.
Fuel Storage Rates in Red Knots
1987; Piersma et al. 1990b). Departures from wintering and staging sites, especially in spring, tend to be highly synchronized at the population level (e.g., Dick et al. 1987). A complete review of the latitudinal locations of the sites used in sequence by the six different subspecies of Red Knots during northward migration is presented in fig. 21.2. There is great variability in the distance traveled by the different subspecies as wintering areas range from the north temperate zone (northwest Europe, subspecies islandica) to the temperate far south (Tierra del Fuego, rufa). Two subspecies (canutus and piersmai) winter in rather tropical climates, with some canutus also going as far south as southern Africa. In addition to the location of the wintering, staging, and breeding areas, fig. 21.2 presents the distances covered by Red Knots in single long-distance flights after departing from the respective areas. Flight distances are always more than 1,000 km, in several cases being more than 6,000 km. To be capable of making such flights, Red Knots need to store considerable quantities of fuel consisting mostly, but not exclusively, of fat (Lindström and Piersma 1993; Piersma 1998; Piersma et al. 1999b; Battley et al. 2000). All else being equal, we would predict fuel stores at departure to be a function of the length of the flights, and fueling rate a function of fuel stores (e.g., Alerstam and Lindström 1990). Data on five of the six subspecies are used here to examine the rates of fuel storage during northward migration at 14 different sites spanning the whole range of latitudes.
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with catches often collected over a series of years; (3) average rates of body mass gain over time for individuals recaptured in different years (in cases where catch averages were not very informative because of relatively low amongindividual synchrony); and (4) a simple comparison between average body mass values early and late in the (re)fueling period. The data used for eight of the 14 sites are presented in fig. 21.3; most of the other data have been published before (see the Appendix to this chapter). In most cases there was a clear break-point in the data to indicate the time-point at which fueling started (especially clear for Delaware Bay, Rio Grande do Sul, and the Wash). The lack of standardization in the data collection and analyses among sites makes it impossible to present confidence limits with the values. In all cases we tried hard to assess the robustness of the values obtained by testing alternative methods of analysis (e.g., regression of individual data points on time vs. calculating average change in body mass for individuals recaptured either in different years or in the same year). We also note that although there are small body-size differences among the subspecies (with the two subspecies wintering in Australasia being somewhat smaller than the others [Tomkovich 1992, 2001]), we have not tried to account for these structural size differences. Without proper analyses of the relationships of body size to mass and to fuel stores, such an exercise would only add further noise to the data. Given the eightfold range in estimated fueling rates (table 21.1), we believe that the estimates are robust enough to make latitudinal comparisons.
MATERIAL AND METHODS We assembled data on body masses of adult Red Knots captured during the period of northward migration (February–May) from as many sites as possible. We did not correct for body mass losses after capture, and, in contrast to passerines, the skin of most shorebirds is too thick to enable the use of visual subcutaneous fat scores (but see Wiersma and Piersma 1995 for the use of indices based on the shape of the abdomen). Only data sets collected over much of the fueling or stopover period would yield estimates of daily rate of mass gain (rate of fueling). As explained in Appendix to this chapter, data sets were screened to remove data points for possible subadult individuals, including individuals that failed to molt into an alternate plumage. Given the large overlap in body size between males and females (Baker et al. 1999), any differences between them have to remain unexamined at this point. However, data on Red Knots staging in Iceland suggest no sex differences in either timing of stopover or fueling rates (Piersma et al. 1999b). Females do store some skeletal calcium, whereas males do not (Piersma et al. 1996a). Fueling rates (in g/day) were based on: (1) regression of individual mass values on the number of days before the average date of northward departure date (for relatively small data sets, usually collected in a single season); (2) regression of average body mass values per catch on the number of days before the average date of northward departure date,
RESULTS The average site-specific fueling rates of Red Knots varied from 0.6 g/day (Golfo San Matias, Argentina) to 4.6 g/day (Delaware Bay, USA) (table 21.1, fig. 21.3), both estimates being based on the same rufa population. Clearly, the refueling rates achieved at the final stopover sites before the flight to the breeding grounds (ranging from 2.7 to 4.6 g/day) were higher than the fueling rates before the first leg of the northward migration from the wintering grounds (0.6–2.8 g/day). Two data points for early stopover sites showed quite a contrast, with rufa knots at Golfo San Matias, Argentina, not gaining more than 0.6 g/day over a month of refueling, and rufa knots in Rio Grande do Sul, Brazil, achieving a refueling rate of 3.1 g/day in the second half of April. The low rate of body mass gain in Argentina was associated with an intense body molt from basic to alternate plumage, combined with birds undertaking a rather short northward flight to northern Argentina and/or southern Brazil (fig. 21.2) (P. M. González et al., unpubl. data). Fueling rates at the low latitudes (around the equator) were lower than at the high latitudes (table 21.1). Perhaps surprisingly, this was not a function of the type of site (initial vs. staging): the fueling rate was correlated with latitude for both the wintering sites as a group as for all sites (fig. 21.4A; the variance explained by absolute latitude was 71%
Fig. 21.2 Schematic resume of the long-distance flights for the six subspecies of Red Knots during northward migration. Nonbreeding areas (thick-lined blocks), staging areas (thin-lined blocks), and breeding areas (shaded blocks) are given in relation to latitude; flight lengths are denoted by arrows and are in kilometers. The subspecies are grouped according to three major flyways, from left to right: the East Atlantic Flyway (islandica, canutus), the East Asian–Australasian Flyway (piersmai, rogersi), and the West-Atlantic (American) Flyway (roselaari, rufa). Note that flight distances are great circle distances, except for the flights from Iceland to northern Ellesmere Island in northeast Canada and the flight from the Wadden Sea to Taymyr Peninsula, both of which are known to more closely follow the rhumbline.
Fig. 21.3 Body mass increases of Red Knots at eight nonbreeding and staging areas before northward migration. Small dots represent individual data points; open circles represent the averages of catches; points joined by lines indicate individual mass trajectories based on catches in different years. These data are summarized in table 21.1, along with the information for the remaining six sites (in five cases based on published information).
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Table 21.1 Summary table of the fueling rates, departure mass, and dates of departure in Red Knots of five subspecies studied at 14 different sites
Subspecies islandica islandica islandica islandica canutus canutus canutus canutus piersmai rogersi rogersi rufa rufa rufa
Site Wadden Sea, Germany Wash, U.K. Balsfjord, Norway Iceland South Africa Guinea-Bissau Mauritania Wadden Sea, Germany NW-Australia New Zealand Victoria, Australia Golfo S. Matias, Argentina Rio Grande do Sul, Brazil Delaware Bay, USA
Type of Site
Latitude
Rate of Refueling (g/day)
Wintering Wintering Final stopover Final stopover Wintering Wintering Wintering Final stopover Wintering Wintering Wintering Early stopover Early stopover Final stopover
53 53 69 65 –33 11 21 54 –18 –37 –38 –41 –31 39
2.8 1.7 2.7 2.9 1.5 0.9 0.7 3.0 0.9 1.2 1.6 0.6 3.1 4.6
Body mass at Departure (g)
Day of Departure (since 1 January)
Length of Fueling Period (days)
191 187 190 211 191 157 168 210 160 185 180 140 180 197
128 123 146 149 108 122 122 152 117 78 83 91 121 151
20 30 21 28 40 70 60 28 57 55 40 37 16 14
Note: Details on the data sources and analyses are presented in the Appendix to this chapter.
for wintering sites only, F1,6 = 14.6, p = 0.01, and 27% for all sites, F1,12 = 4.4, p < 0.06). The estimated body mass at departure on subsequent northward flights was also a function of latitude (fig. 21.4B; variance explained by absolute latitude was 42%, F1,12 = 8.8, p = 0.01), but, surprisingly, was not correlated with the estimated length of the ensuing flight (from fig. 21.2; F1,12 = 0.03, p = 0.86). Interestingly, the correlation between fueling mass and fueling rate was relatively strong (fig. 21.4C; variance explained was 55%, F1,12 = 14.5, p = 0.003). Finally, both fueling rate and departure mass were strongly correlated with the estimated length of the fueling period (variances explained were 69%, F1,12 = 26.9, p < 0.001 and 33%, F1,12 = 5.9, p = 0.03, respectively).
DISCUSSION Is Comparing Gross Fueling Rates among Sites Justifiable? This review is based on a comparison of whole body mass values. Because the contributions of wet protein and fat to the body mass, gains may vary among species (Lindström and Piersma 1993; Piersma 1998), and even within species depending on the time of year (Piersma and Jukema 2002), the fueling rates may not be directly comparable in terms of energy equivalents. For Red Knots staging in Iceland we know that fat contributed 78% to the total mass increase during the stopover (Piersma et al. 1999b) and a similar estimate is now available for birds staging in Delaware Bay (T. Piersma et al., unpubl. data). However, for all the other staging sites this information is lacking. Variability in fuel composition among sites could be compounded by temporal variability in the composition of fuel
stored and variability in storage rates in the course of a stopover. Studies of islandica knots from the Icelandic site (Piersma et al. 1999b) reveal that fueling rates are relatively low during the first week of stopover and consist mainly of wet protein (reflecting the buildup of “digestive” organs such as the gut and liver). This is followed by a phase of rapid mass gain (much of which consists of fat), followed by a final phase of a slower mass gain during which wet protein is lost (reflecting the balance between the breakdown of the digestive systems and the buildup of “exercise” organs such as pectoral muscles and heart) and only fat is gained. As the energy equivalent of fat is eight times higher than that of wet protein ( Jenni and Jenni-Eiermann 1998), differences in fuel composition among sites and times should ideally be taken into account in discussions of the ecological factors promoting differences in fueling rates. For now, we assume that the composition of the fuel stored during northward migration is similar among sites and, thus, that the energy intake necessary to deposit a gram of fuel is a constant proportion of the estimated fueling rate across all sites.
Evidence for the Use of Time-Minimization Strategies As outlined by Alerstam and Lindström (1990), migrants using a time-minimization strategy are predicted to have fuel loads at departure (departure masses) that are a positive function of fueling rates. Such a relationship should be absent in energy-minimizing migrants. In a comparison between species-average values for shorebirds and passerines, Alerstam and Lindström (1990) found positive correlations between fuel loads at departure and fueling rates in both groups of birds, which they interpreted as evidence for the
Fuel Storage Rates in Red Knots
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parison (between individual and species-specific values), but confirm once again the predicted positive correlation between fuel load at departure and fueling rate expected for time-selected migrants. Optimal migration theory (Alerstam and Hedenström 1998) would also predict that the fuel load at departure, all else being equal, would be a function of the length of the ensuing migration flight. As this relationship appears absent, we must conclude that “all else” is not equal, and that the degree of wind assistance (Piersma and van de Sant 1992; Green 2003), the type of flight (transoceanic or not, Piersma 1998), the extent of organ mass reductions before departure (Piersma 1998), the degree to which an increasing fuel load increases the cost of flight (Kvist et al. 2001), as well as the expected ecological conditions upon arrival vary among flights and perhaps among populations.
Latitudinal Trends
Fig. 21.4 Relationships between (A) population average fueling rates and absolute latitude, (B) average departure mass and absolute latitude, and (C) average departure mass and refueling rate for Red Knots (based on data in table 21.1). Note that open circles indicate wintering sites from which northward migration is started, triangles indicate early stopover sites, and filled circles indicate final stopover sites before the flight to the breeding grounds. The regression line in the plot of fueling rate versus absolute latitude is for the wintering sites only.
quite general use of time-minimization strategies. In a follow-up study, Lindström and Alerstam (1992) were able to obtain qualitative agreement between the predictions based on the time-minimization strategy and the individual fueling rates and departure masses in two passerine species. Our data on estimated population-average take-off masses and fueling rates for Red Knots belonging to different subspecies at different sites occupy the middle stratum of com-
The thermal environment for Red Knots would appear to be rather more favorable at tropical latitudes than at (north) temperate latitudes. In fact, there is a strong negative correlation between estimated average air temperatures and absolute latitude for the 14 fueling events reported here, with air temperatures going down by 0.4°C for every degree of latitude (r = 0.93, F1,12 = 78.7, p < 0.001). At tropical latitudes Red Knots experience average air temperatures of 25°–30°C, whereas in Iceland and northern Norway they have do deal with averages of 5°–10°C. This implies a twofold difference in the maintenance costs between highand low-latitude fueling sites (Wiersma and Piersma 1994; Piersma 2002). Everything else being equal (time-activity budgets, cost of food acquisition, handling and processing, harvestable food abundance, energy density of stored tissue, efficiency of night- and daytime feeding), one would expect Red Knots at circa-tropical sites to have higher, rather than lower, fueling rates than Red Knots at high-latitude sites (Lindström 1991). The beauty of ecological studies of Red Knots is that these birds have highly specific habitat requirements, which leads to ecological similarities between most wintering and staging sites. The diet consists mainly of molluscs, and birds follow a tidal rhythm with two 6-h bouts of foraging during low tide. The exception (to both rules) is in Delaware Bay, where knots eat the eggs of horseshoe crabs (Limulus polyphemus [Tsipoura and Burger 1999, pers. obs.]), during the 12 h of daytime (pers. obs.). At Lagoa do Peixe, Rio Grande do Sul, Brazil, Red Knots make use of ocean beaches as well as semitidal lagoon; here birds could be less constrained by time and tide. With diet and time budgets being so comparable between high- and low-latitude sites, it makes sense to argue that the surprising trend between latitude and fueling rates must be due to external factors. Although at midday Red Knots in the Tropics may incur some heat stress (Battley et al. 2003), it is unlikely that external heat loads over the entire day could put a constraint on foraging activity (which
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itself leads to heat production [Verboven and Piersma 1995; Bruinzeel and Piersma 1998]). The remaining ecological factor that could explain the observed pattern in fueling rates is that there may be a constraint on the rate of food intake that becomes more severe at the lower latitudes. Red Knots fueling in captivity have been shown to achieve fueling rates far above what have been documented in the field, suggesting that food intake in the wild may be constrained at all sites. When canutus knots that are migrating through the Baltic (and are therefore highly motivated to eat) are put in cages where they can eat as much high-quality soft food (mealworms Tenebrio sp.) as they want, they routinely achieve fueling rates of 10 g/day and higher (Kvist and Lindström 2003). In view of the significant positive correlation between the total benthic biomass at intertidal flats and absolute latitude (for 14 sites where Red Knots occur, r = 0.56, F1,12 = 5.3, p = 0.04; most data are from Piersma et al. 1993a [table 21.1]) and the finding that the few available direct estimates of intake rate indeed indicate that food, from the point of view of the Red Knots, is most abundant at southern and northern high-latitude sites (G. B. Escudero, unpubl. data), the severity of a constraint on food intake may be stronger in the Tropics than elsewhere. However, establishing the extent to which higher intake rates at high-latitude staging sites can more than compensate for the increase in energy expenditure (due to a less favorable thermal environment) requires detailed energy budget reconstructions for Red Knots at a good range of sites (see Alerstam et al. 1992; Piersma et al. 1994; González et al. 1996). In addition, variations in prey quality (e.g., the amount of digestible flesh per unit ingested shell mass) determines the extent to which the birds face digestive rather than gross-intake bottlenecks (van Gils et al. 2003a).
fueled birds) are relatively scarce (see Ydenberg et al. 2002)? Or do the patterns reflect simple fitness optimization rules based on assumptions on the relative “fueling qualities” of the different sites (Weber et al. 1998)? To determine whether changing food abundance at staging sites affects fueling performance and even the subsequent use of stopover sites, we need large-scale experiments. Actually, the time seems ripe to take scientific advantage of unfortunate human-induced alterations to the staging sites of Red Knots, the usual story of overfishing and the concomitant loss of marine resources (e.g., Piersma and Baker 2000; Piersma et al. 2001; A. J. Baker et al. 2004[AQ1]), by monitoring both food abundance and bird responses. In addition, we may be able to determine which fueling rates are preferred by individual Red Knots at particular sites and times of the year by experimentally measuring rates of food intake and mass gain under captive conditions with an unlimited high-quality food supply (as in the study of Kvist and Lindström 2003). Such a combination of experimental field and laboratory studies in the context of the descriptive framework set up here may for the first time enable us to disentangle the ecological and physiological factors that determine fueling rates of shore- and other birds, assess the patterns in a theoretical context (Alerstam and Hedenström 1998), and determine how ecology and physiology combine to affect the fitness of long-distance migrants. For example, how and to what extent is physiological flexibility used to buffer ecological variance?
APPENDIX: DETAILS OF DATA SOURCES AND ANALYSES Data for both the subspecies islandica and canutus were collected from 1978 to 1987 (usually based on large cannon-net catches) and summarized by Prokosch (1988).
WADDEN SEA, GERMANY.
FUTURE DIRECTIONS: DISENTANGLING ECOLOGICAL CAUSES AND PHYSIOLOGICAL EFFECTS Red Knots must arrive on their High Arctic breeding grounds at the right time and with the right remaining energy and nutrient stores. These stores appear to be used for survival (note that late springs have led to major mortality [Boyd 1992]) rather than the actual production of eggs (Klaassen et al. 2001), although the calcium for eggshell is strategically stored (Piersma et al. 1996b). In fitness terms, everything else in the annual cycle may be subservient to arrival timing (Drent et al. 2003). Because the staging times are shortest and the fueling rates are highest at the last stopover sites before the High Arctic, there appears to be rather little “slack” time at late stages in the migration. Does this indicate that the time-energy budgets are also tight earlier in the year (restricting the departure times from the south)? Or does it reflect the presence of late-opening “time windows of opportunity” when food is abundant (Myers 1986) and/or dangerous predators (especially for fully
WASH, UK. Based on a regression on date of 525 data points for adult Red Knots captured within 30 days of the departure date, having excluded individuals with little evidence of molt into an alternate plumage (that were always lightweight). Data were made available from the period March–May 1969–1991 by the Wash Wader Ringing Group (WWRG and J. Clark et al., unpubl. data; Y. Verkuil, pers. comm.). BALSFJORD, NORWAY. Data obtained on the basis of a series of cannon-net catches in May 1985 that were summarized by Davidson and Evans (1986).
All date-specific average body mass values obtained between 2 and 30 May (in 1970, 1971, and 1972 and the mid-1980s) and published in Gudmundsson et al. (1991:fig. 4) and Piersma et al. (1999b:table 1) were used as a basis for a linear regression. See also Wilson and Morrison (1992).
ICELAND.
Fuel Storage Rates in Red Knots
SOUTH AFRICA. Data were obtained between 1970 and 1977 (mostly based on mist-net catches) and were summarized for monthly or biweekly intervals by Summers and Waltner (1978:fig. 4). GUINEA-BISSAU. Based on the original data collected by WIWO-volunteers and associates in 1993 (see Wolff 1998). We regressed body mass values for adults on time of year (excluding individuals not molting into an alternate plumage) and used observations of departing flocks to calculate average date of departure. BANC D’ARGUIN, MAURITANIA. Based on the original data collected by WIWO-volunteers and associates in 1985, 1986, and 1988 (see Zwarts et al. 1990b). We regressed body mass values for adults on time of year (excluding late birds with very little alternate plumage and aberrantly low body masses) and used observations of departing flocks (Piersma et al. 1990a) to obtain an estimate of the average date of departure.
Based on 21 body mass values of adult birds captured with cannon-nets in Roebuck Bay near Broome in different years at least 6 days apart (data collected between 1985 and 2001). Data were collected by the Australasian Wader Study Group.
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ACKNOWLEDGMENTS
Red Knots in all parts of the world have attracted many marvelous, dedicated field workers working in both amateur and professional capacity. Even if this chapter shows that we need further research efforts, it is a tribute to their diligence. We sincerely thank all helpers in the field and the funding agencies that over many years made the work possible. The first author thanks Pete Marra, Russ Greenberg, and the Smithsonian Institution for enabling this contribution, and the Netherlands Organization for Scientific Research (NWO) for funding shorebird and benthic research over an extended period of time with a PIONIER grant. Similarly, work in the Western Hemisphere on rufa knots has been funded on a continuing basis by the Royal Ontario Museum Foundation and the Natural Sciences and Engineering Research Council of Canada (NSERC) to AJB. We thank Åke Lindström, Phil Battley, the editors, and two anonymous referees for comments on drafts, Dick Visser for drawing the final figures, and Jan van de Kam for use of his photographs.
NW AUSTRALIA.
Based on a comparison of average masses from cannon-net data collected between 1987 and 1993 summarized by Battley (1999).
NEW ZEALAND.
Based on a comparison of average masses in (different season) cannon-net catches on 21 February and 22 March made near Melbourne (data collected between 1987 and 1999). Data were collected by the Victorian Wader Study Group.
VICTORIA, AUSTRALIA.
Linear regression of individual data points based on a series of five cannonnet catches of a total of 890 adult birds near the town of San Antonio Oeste, Rio Negro, in March 1998.
GOLFO SAN MATIAS, ARGENTINA.
LAGOA DO PEIXE, RIO GRANDE DO SUL, BRASIL.
Based on body mass values of Red Knots mist-netted by teams of CEMAVE near Lagoa do Peixe in April 1997, 1999, 2001, only using the data from the latter half of the month when the population shows a steep (synchronous) rate of refueling. Based on data collected during 63 cannon-net catches by an international consortium from 1997 to 2001 in New Jersey as well as Delaware (Niles et al., unpubl. data). A linear regression on date of average body mass values per catch-day between 14 and 30 May was used to estimate the overall rate of refueling
DELAWARE BAY, USA.
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