
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northward migration, based on published and unpublished data collected in South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
262
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
263
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-
264
             
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.
265
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).
268
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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
269
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
270
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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.
271
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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Possible to supply 300-dpi graphics files for figure 21.1, to improve appearance?