Extended primary moult as an adaptation of adult
Wood Sandpipers Tringa glareola to their freshwater habitats
in southern Africa
Magdalena Remisiewicz1,2,*, Anthony J. Tree3, Les G. Underhill1,
Anna Gustowska2 & P. Barry Taylor4
Remisiewicz M., Tree A.J., Underhill L.G., Gustowska A. & Taylor P.B. 2009.
Extended primary moult as an adaptation of adult Wood Sandpipers Tringa
glareola to their freshwater habitats in southern Africa. Ardea 97(3): 271–280.
Migrant waders using freshwater habitats are hypothesized to have slower primary moult than waders using coastal habitats. We chose the Wood Sandpiper
Tringa glareola as a representative species using the freshwater habitats and
compare its moult pattern with a range of fresh-water and coastal wader
species to test the habitat hypothesis. Only fragmentary descriptions of Wood
Sandpipers’ primary moult in their sub-Saharan non-breeding quarters had
existed. We analysed the primary moult formulae of 1496 adult Wood Sandpipers obtained in southern Africa. The Underhill & Zucchini moult model was
used to estimate the timing and duration of moult for all 10 primaries combined
and for each primary individually. We also estimated the rate of production of
feather material during moult. Adult Wood Sandpipers arrive in southern Africa
between late July and November, and depart from mid-March to April.
Suspension of moult was observed in 56 birds (7.5%) after two to nine primaries had been replaced. The remaining birds performed a continuous complete
primary moult, with average start and completion dates of 21 August and 30
December, respectively; estimated duration was 131 days. The overall rate of
production of primary feather material was uniform, achieved by growing up to
five small inner primaries simultaneously at the beginning of the moult but only
one or two simultaneously while the large outer primaries were growing.
Primary moult of adult Wood Sandpipers took longer but ended earlier than in
similar-sized waders using coastal habitats. Compared with waders using
coastal habitats, Wood Sandpipers prolonged moult by shedding their primaries at longer intervals and by extending the growth period of each primary. The
longer primary moult and its earlier ending compared with coastal waders are
probably adaptations to Wood Sandpipers’ use of freshwater habitats, which in
southern Africa provide unpredictable food supplies and might require nomadic
movements between ephemeral inland wetlands.
Key words: Wood Sandpiper, Tringa glareola, primary moult, southern Africa,
shorebirds
1
Animal Demography Unit, Department of Zoology, University of Cape Town,
Rondebosch 7701, South Africa; 2Avian Ecophysiology Unit, Department of
Vertebrate Ecology and Zoology, University of Gdańsk, al. Legionów 9, 80-441
Gdańsk, Poland; 3Department of Zoology, Nelson Mandela Metropole
University, P.O. Box 1600, Port Elizabeth 6000, South Africa;
4
School of Biological and Conservation Sciences, University of KwaZulu-Natal,
Private Bag X01, Scottsville 3209, Pietermaritzburg, South Africa;
*corresponding author (biomr@ug.edu.pl)
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ARDEA 97(3), 2009
INTRODUCTION
Different life histories have been suggested for waders
using coastal and freshwater habitats with consequential contrasting attributes such as migration distances,
genetic variability and immunocompetence (Piersma
1997, 2003). Moult, being an important part of the lifecycle and migration strategy, might also differ between
species that use coastal and inland wetlands. A variety
of primary moult strategies has been described for
long-distance migrant waders in relation to their breeding success, migration distance, or the latitude they
may reach in the non-breeding season (Prater 1981,
Ginn & Melville 1983). Most detailed studies of moult
patterns have been on tundra-breeding waders that
migrate to coastal habitats: Ruddy Turnstone Arenaria
interpres (Summers et al. 1989), Grey Plover Pluvialis
squatarola (e.g. Serra et al. 1999, Serra & Underhill
2006), Sanderling Calidris alba (Summers et al. 1987,
Underhill 2003), Purple Sandpiper C. maritima
(Morrison 1976, Summers et al. 2004), Curlew Sandpiper C. ferruginea (Minton et al. 2006). This can be
attributed to large-scale ringing at coastal localities,
combined with the developing methodology of moult
studies (Underhill & Zucchini 1988, Underhill et al.
1990, Underhill 2003, Underhill et al. 2006). In contrast, moult patterns of species that breed in the taiga
and use freshwater inland wetlands in the non-breeding season have been poorly studied because of limited
material available on these widely dispersed birds.
Waders using freshwater wetlands are predicted to
need a longer and more flexible strategy because these
irregular habitats provide unpredictable food resources
(Piersma 2003), in contrast to waders relying on the
abundant and predictable food supplies of marine habitats (Velasquez et al. 1991, Hockey et al. 1992,
Underhill 2003, van de Kam et al. 2004).
We expect that the Wood Sandpiper Tringa glareola
represents the group using freshwater habitats. Wood
Sandpiper populations of the African-Eurasian migration system breed in the taiga from Fennoscandia to
western Siberia. Their non-breeding grounds are the
wetlands of sub-Saharan Africa, including the mesic
northeastern part of southern Africa (Cramp &
Simmons 1983, Lebedeva et al. 1985, Underhill 1997,
Underhill et al. 1999). Unlike many wader species in
which first-year birds skip their first breeding opportunity, most first-year Wood Sandpipers return to the
breeding grounds aged about nine months, a factor
which simplifies the analysis (Summers et al. 1995,
Underhill 1997, 2006). Though the Wood Sandpiper is
often abundant at stopover and non-breeding grounds,
descriptions of its moult are fragmentary and do not
provide a wider overview (Hoffmann 1957, Tree 1974,
Pearson 1974, Ginn & Melville 1983, Pinchuk et al.
2008).
This paper has two aims. (1) To identify the adult
Wood Sandpiper’s strategy for primary moult in the
southernmost part of its non-breeding range by
analysing a large data set of moult records collected in
southern Africa since 1900. (2) To verify the hypothesis
that the Wood Sandpiper’s primary moult has distinctive attributes related to its use of freshwater habitats
which contrast with those of waders using coastal habitats in southern Africa.
METHODS
We analysed the primary moult formulae of 1496 adult
Wood Sandpipers from three sources: 116 specimens
from the National Museum of Zimbabwe in Bulawayo
collected in 1900–1975 and examined by AJT; 1277
birds ringed in southern Africa in 1966–1999 by AJT,
and 103 birds ringed in 2001–2007 by PBT (with MR
and AG in 2007). Most of the museum specimens originated from Zimbabwe, with a few from Botswana. Data
on live birds were obtained from irregular mist-netting
at wetlands in Zimbabwe and South Africa (Fig. 1). The
state of moult in the primaries of one wing was
recorded as a moult formula, a string of 10 digits, one
for each primary, following the standard approach:
scores of 0 and 5 indicate old and replaced feathers,
respectively, and intermediate values describe growth
stages (Ashmole 1962, Ginn & Melville 1983).
Wood Sandpipers were aged by their plumage as
first-year, second-year, or adult birds. First-year and
second-year birds (up to c. 18 months) were aged by
the retained juvenile-type inner median coverts or by
the contrast between two generations of primaries
showing partial moult (Prater et al. 1977, MR unpubl.
data). From about December of their second year
immatures become indistinguishable from adults. Birds
aged as second-year birds were excluded from this
analysis; however, our sample contains a small number
of unidentified second-year birds, especially among
those captured after December. Most of these birds had
completed migrations to and from the breeding
grounds, and their moult is likely to have become synchronized with the adults.
Only the moult formula described at the first capture
of an individual in a season was used in estimating
moult parameters. Moult records were pooled, assuming they were representative of all southern African
273
Remisiewicz et al.: MOULT OF WOOD SANDPIPERS IN SOUTHERN AFRICA
10°E
20°E
30°E
40°E
10°S
Zimbabwe
(1171)
20°S
South Africa
N
(208)
30°S
Figure 1. Catching sites of Wood Sandpipers in Zimbabwe and
South Africa. The number of birds from each country are shown.
birds. The date of capture or collection was taken as the
number of days from 1 June; records from all years
were combined because we lacked sufficient data from
any year to estimate annual moult parameters. Birds
with suspended moult (e.g. a moult formula of
5550000000, with no growing feathers) were distinguished from those in continuous moult (scores of 1, 2,
3 or 4 in the moult formula). Birds that had suspended
and then resumed moult could not be identified by the
moult formulae.
Two approaches were used to obtain the starting
date of primary moult and its duration for birds in continuous moult. Firstly, we followed Summers et al.
(1989, 2004), Underhill & Summers (1993) and Serra
et al. (1999) and used the Underhill & Zucchini (1988)
model to analyse the entire tract of 10 primaries combined. Moult data were of Type 2 (Underhill & Zucchini
1988) because most adult Wood Sandpipers had not
commenced moult on arrival in August to October and
they were available for sampling of moult (Fig. 2). The
exceptionally early moulters were a few so they hardly
influenced the results. From the moult formula we cal-
culated the Proportion of Feather Mass Grown (PFMG)
(Underhill & Summers 1993). Assuming primary
feather tissue is deposited at a continuous rate, this
provided the moult index required by the Underhill &
Zucchini (1988) model. The calculation of PFMG from
the moult formula (Underhill et al. 1993, Underhill &
Joubert 1995) requires the mean relative mass of each
primary; to obtain this we weighed the dried primary
feathers of six dead adult Wood Sandpipers, and averaged the relative masses for each primary (Table 1).
Moult parameters (mean starting date, standard deviation of mean starting date, and moult duration) were
estimated using the software described in Brandão
(1998) and in Underhill et al. (2006). The confidence
limits for the moult starting date (when 95% of birds
had started to moult) were calculated as the estimated
mean starting date ± 1.96 x standard deviation.
Secondly, we used the Underhill & Zucchini (1988)
model to estimate the moult parameters of individual
primaries (as in Underhill 2001, 2003, Serra 2002,
Serra & Underhill 2006, Underhill et al. 2006). For each
primary we created a moult index by transforming its
score of 0 to 5 in the moult formula to the values 0,
0.125, 0.375, 0.625, 0.875 and 1 respectively, as
described by Serra (2002) and Underhill (2003). The
date the first (innermost) primary (P1) started to moult
was taken as the date primary moult commenced and
the date the outermost primary (P10) ended moult was
taken as the date it finished.
The growth rate of the primary feather tract, estimated by the Underhill & Zucchini (1988) model, was
compared with the growth rates of primaries calculated
from the increase of the PFMG of 16 individuals caught
twice in the same season. We computed the weighted
average of the difference between the two PFMG values, using the intervals between capture as weights.
The ratio of the relative mass of each primary to its
estimated duration of moult provides an estimate of its
daily growth rate (units: % PFMG/day). Using these
values and the estimated starting and ending dates of
moult for each primary, we estimated the daily increments of PFMG for each feather during moult. We
summed these increments for each calendar day. This
Table 1. Relative masses of Wood Sandpiper primaries expressed as a percentage of the total mass of primary feathers, based on the
weights of primaries of six individuals caught in 2003–06 during northward passage in Poland (W. Meissner, L. Pilacka, P. Gogga in
litt.).
Primary
Relative mass (%)
P1
P2
P3
P4
P5
P6
P7
P8
P9
P10
4.58
5.34
6.23
7.20
8.81
10.72
12.10
13.61
14.93
16.48
274
ARDEA 97(3), 2009
enabled us to model, for the average bird, the daily production rate of primary feather material and to plot the
cumulative growth during moult. If the underlying
assumption of the Underhill & Zucchini (1988) moult
model is correct, the plot of daily growth values should
be constant and the cumulative growth curve should be
linear.
We also estimated the Proportion of Feather Mass
Missing (PFMM), providing a measure of the size of the
gap in the primary feathers during moult that takes
into account the relative sizes of the missing feathers.
To calculate PFMM we used an approach that is complementary to the calculation of PFMG: feathers with
moult scores of 1, 2, 3 and 4 are taken as representing
0.875, 0.625, 0.375 and 0.125 respectively of the missing relative mass of each primary. We used these values
for growing feathers as shown by the moult formula,
following Ward et al. (in press). PFMM is a refinement
of the raggedness score of Haukioja (1971) and Bensch
& Grahn (1993); raggedness is based only on the moult
formula, whereas PFMM takes account of the relative
sizes of the feathers.
26 October, 4400000000 on 26 November and
5555552100 on 30 January. For Data Type 2 of the
Underhill & Zucchini (1988) moult model we included
the individuals in active moult (excluding the four outliers), birds that had not started to moult and the birds
that had finished moulting, a total sample of 1435
(Fig. 2).
The mean starting date of the primary feather tract
moult was estimated to be 21 August; the mean starting date of moult of P1 as an individual primary was 22
August (Table 3). The mean completion dates of primary moult as estimated by the two methods differed
by two days: 28 December (completion date of moult
of P10) and 30 December (based on the primary
feather tract) (Table 3).
The standard deviation of the starting date estimated for the primary tract was 29 days (Table 3), thus
the estimated period during which 95% of birds started
moult was 112 days between 25 June and 16 October
(Fig. 2). Similarly, 95% of adults completed primary
moult between 3 November and 24 February. The
period between the start of moult of P1 and the end of
Pattern and timing of primary moult
The earliest date an adult Wood Sandpiper was caught
after arrival was 16 July; four birds had already started
to moult by the end of July (Fig. 2). Of the 1496 Wood
Sandpipers ringed and examined between July and
May, 7% had not yet started to moult, 50% were in
moult and 43% had completed their moult (Fig. 2). Of
746 birds in moult, 56 (7.5%) had suspended moult
after 2–9 inner primaries had been renewed. 95% of
birds with suspended moult were observed between 4
and 23 November; 57% of suspension occurred after
seven or eight inner primaries had been replaced
(Table 2).
The remaining 690 birds in active moult showed
continuous moult of the primaries, starting at P1 and
progressing outwards to P10. The PFMG values of four
individuals were identified by the model as outliers:
formula 0000000000 on 24 October, 5555555554 on
proportion feather mass grown (PFMG)
RESULTS
1.0
0.8
0.6
0.4
0.2
N = 1435
0.0
Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May
Figure 2. Temporal distribution of the Proportion of Feather
Mass Grown (PFMG) of adult Wood Sandpipers in southern
Africa. The continuous line shows the timing of moult for an
average bird, the dashed lines show estimated confidence intervals between which 95% of birds caught on a particular date
ought to fall.
Table 2. Percentages of adult Wood Sandpipers that renewed feathers given below before the suspension of moult in southern Africa
(n = 56).
Primaries moulted
Percentage
P1–P2
P1–P3
P1–P4
P1–P5
P1–P6
P1–P7
P1–P8
P1–P9
4
0
2
14
12
25
32
11
275
Remisiewicz et al.: MOULT OF WOOD SANDPIPERS IN SOUTHERN AFRICA
moult of P10 was estimated to be 128 days; based on
the primary feather tract the estimated duration of
moult was 131 days.
The average moult rate calculated for 16 individuals
caught twice in one season was 0.77 PFMG/day (SD =
0.19). This suggested a primary moult duration of 130
days. The average of the estimated moult period for six
of these birds trapped more than 30 days apart was 126
days (SD = 31 days). These results confirm the duration
of moult obtained by using the moult models.
Moult parameters of individual primaries
The estimated duration of growth for each of the primaries varied from 20 to 31 days (Table 3, Fig. 3). The
daily growth rates of the smaller primaries P1 to P4
were about two or three times slower than of the
largest P9 and P10 (Table 3, final column). This is
shown by the steeper growth lines for the outer primaries than those for the inners (Fig. 3). During the
replacement of P1–P4 on average the number of feathers growing simultaneously was larger than three and
4
P10
number of growth primaries
relative mass of primary (%)
16
12
P5
8
4
0
112
117
101
3
114
118
2
142
176
P7
P8
151
143
1
0
Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May
113
P1
P2
P3
P4
P5
P6
P9 P10
number of shed primary
Figure 3. Dates of the start and the end of moult of individual
primaries (P1–P10) moulted by adult Wood Sandpipers in
southern Africa. The endpoints of lines are at the relative mass
of each primary so that the slopes of the lines represent the
growth rates of the primary.
Figure 4. The mean number of simultaneously growing primaries while each of the 10 primaries is in moult. Sample sizes and
95% confidence intervals for the mean are shown.
Table 3. Estimates of moult parameters of each primary and of the 10 primaries as a single tract for adult Wood Sandpipers in southern Africa. The final column provides the estimated daily growth rate of each primary, calculated from the relative feather mass
(Table 1) and the estimated moult durations.
Moult parameters
Primary
Sample sizes
Mean start
date (SD)
Duration
(SD)
Standard
deviation of
start date (SD)
End date
(SD)
Not yet
moulted
In
moult
Moult
complete
% PFMG /
day
P1
P2
P3
P4
P5
P6
P7
P8
P9
P10
22 Aug (1.6)
23 Aug (1.5)
28 Aug (1.6)
7 Sep (1.5)
17 Sep (1.5)
27 Sep (1.5)
11 Oct (1.6)
27 Oct (1.7)
16 Nov (1.7)
2 Dec (1.8)
25 (1.9)
25 (1.9)
25 (1.9)
20 (1.7)
21 (1.7)
21 (1.7)
25 (1.8)
31 (1.9)
27 (1.9)
26 (1.9)
19 (1.1)
19 (1.1)
20 (1.1)
21 (1.1)
20 (1.0)
21 (1.0)
26 (1.2)
30 (1.2)
32 (1.3)
34 (1.3)
16 Sep (1.5)
17 Sep (1.1)
22 Sep (1.5)
27 Sep (1.5)
8 Oct (1.4)
18 Oct (1.4)
5 Nov (1.5)
27 Nov (1.7)
13 Dec (1.7)
28 Dec (1.8)
108
114
136
183
224
273
350
440
556
650
109
108
108
89
105
113
140
178
152
145
1218
1213
1191
1163
1106
1049
945
817
727
640
0.18
0.21
0.25
0.36
0.42
0.51
0.48
0.44
0.55
0.63
P1–P10
21 Aug (1.7)
131 (2.5)
29 (0.8)
30 Dec (1.4)
108
687
640
0.76
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ARDEA 97(3), 2009
growth during moult was nearly linear (Fig. 5). The
intervals between which the quartiles of PFMG were
achieved were similar (Fig. 5). This indicates that
PFMG increased at an almost constant rate.
cumulative %PFMG/day
100
80
102 days
60
65 days
40
33 days
20
21.08
26.08
31.08
5.09
10.09
15.09
20.09
25.09
30.09
5.10
10.10
15.10
20.10
25.10
30.10
4.11
9.11
14.11
19.11
24.11
29.11
4.12
9.12
14.12
19.12
24.12
0
date
Figure 5. The cumulative Proportion of Feather Mass Grown
(PFMG) during moult. The straight line shows a uniform growth
rate. The dashed lines represent the dates on which the quartiles
of PFMG are reached; the number of days from the start of
moult taken to reach each quartile is given.
Size of the wing gap during primary moult
The mean size of the wing gap described by PFMM was
0.10 (SD = 0.056, range 0.01–0.03), so that, on average, birds were missing 10% of their primary flight
feathers’ mass during moult (Fig. 6). The two largest
values were 0.33: one bird was replacing its three outer
primaries (formula 5555555311 on 11 January), and
an exceptional bird was recorded with seven actively
growing primaries (formula 5554443322 on 13
November). In birds with active moult, the Proportion
of Feather Mass Missing (PFMM) was negatively correlated with PFMG (r = –0.19, P < 0.001) so that gaps
tended to be larger at the start of moult than at the end.
proportion feather mass missing (PFMM)
DISCUSSION
0.3
0.2
0.1
0.0
0.0
0.2
0.4
0.6
0.8
1.0
proportion feather mass grown (PFMG)
Figure 6. The relationship between the size of the gap in the primaries during moult, expressed as a Proportion of Feather Mass
Missing (PFMM) and Proportion of Feather Mass Grown
(PFMG). The pattern of parallel lines is a consequence of the recording of moult scores for individual feathers to integer values.
during the replacement of P6–P10, the average was less
than two (Fig. 4). For P1–P5, the estimated intervals
between shedding successive primaries were 1–10 days
(mean 7 days), and for P6–P10 they were 10–20 days
(mean 15 days) (Table 3, Fig. 3).
Rate of primary feather mass production
Using daily production rates of primary feather material for each individual primary (Table 3, final column)
and considering the overlapping growth of neighbouring primaries, the plot of the cumulative feather mass
Pattern and timing of moult
More than 90% of adult Wood Sandpipers that migrate
to southern Africa performed a continuous complete
moult of their primaries. This confirms previous studies
which indicate most adult Wood Sandpipers moult only
after reaching the non-breeding grounds (Tree 1974,
Ginn & Melville 1983). The estimated mean date for
the start of moult, 21 August, and the upper limit of the
95% confidence interval, 16 October (Fig. 2), correspond with the stated arrival period of Wood Sandpipers in southern Africa, from late-July but mostly
August-September (Underhill 1997, Oschadleus 2002).
The lower limit of the confidence interval for the starting date of moult was 25 June (Fig. 2), earlier than the
accepted date of arrival in southern Africa.
Reconsideration of the modelled reporting rates for
Wood Sandpipers in Zimbabwe (Zone 5 in Underhill
1997) shows that reporting rates increase from July
and became stable in early October, with arrivals progressively later farther south and east in southern
Africa. Given that most birds in this study were captured in Zimbabwe, the lower confidence interval of
the starting date of moult is consistent with the early
arrival of failed breeders. Overall, the pattern suggests
that most migrants commence primary moult shortly
after arriving in southern Africa. Thus the 112-day 95%
confidence interval for the start of moult probably
reflects a genuine lack of synchronisation of moult.
Wood Sandpipers migrate to southern Africa from
breeding grounds stretching from Scandinavia to west-
Remisiewicz et al.: MOULT OF WOOD SANDPIPERS IN SOUTHERN AFRICA
ern Siberia (Underhill et al. 1999), so they migrate
between c. 8 000 km and 12 000 km. This is probably
another reason for the extended period of arrival
(Underhill 1997); and consequently the prolonged
period over which they begin their moult.
The end of primary moult was estimated, on average, to be late December; departure on northward
migration does not take place until mid-March or April
(Underhill 1997, Hockey et al. 2005). Waders which
use mainly coastal habitats, such as Knot, Sanderling,
Ruddy Turnstone and Grey Plover, finish moulting their
primaries in southern Africa in January or February
(Serra et al. 1999, Underhill 2003) and depart for their
breeding grounds one to two months later, in March
and April (Hockey et al. 2005). Coastal birds can rely
on a fairly constant food supply at tidal mudflats while
accumulating reserves before migration (Velasquez et
al. 1991, Hockey et al. 1992, Underhill 2003, van de
Kam et al. 2004). Wood Sandpipers have two to three
months between the completion of primary moult and
their departure. During this period the Wood
Sandpipers continue replacing other feather tracts,
such as secondaries, tertials and rectrices, accumulate
reserves and acquire breeding plumage before migration (Ginn & Mellville 1983, AJT, MR unpubl. data).
The longer period for these activities compared with
coastal waders is probably an adaptation to their use of
unpredictable food resources at freshwater habitats
(Piersma 2003) and their possible need to move
between suitable wetlands. In northeastern southern
Africa, where Wood Sandpipers mostly occur, the end
of moult coincides with the wettest part of the rainy
season. As wetlands fill they become unsuitable for
waders, necessitating movements to regions with less
rainfall, mainly to the more arid western and southern
parts of the region (Underhill et al. 1999). Ringing
recoveries of Wood Sandpipers confirm these nomadic
movements between inland wetlands while staging in
southern Africa before their return migration (Underhill
et al. 1999, SAFRING unpubl. data)
A small proportion of adult Wood Sandpipers
caught in southern Africa showed suspended moult.
The moult starting dates estimated from the sample of
all primaries combined (which might include birds that
resumed moult after its suspension before they arrived
in southern Africa) and on the moult data for P1
(which did not include such birds) were almost identical, which shows that cases of undetected suspended
moult were so few that they did not bias the estimates
obtained from the first method. Most of the birds with
moult suspension were observed in southern Africa in
November, three months after the start of moult, at a
277
time when birds undergoing continuous moult were
replacing their outer three primaries (Table 3). It is
likely that they suspended moult on the non-breeding
grounds, perhaps in response to a need to move to a
suitable wetland. Wood Sandpipers moulting or with
suspended moult were observed rarely in August or
September in eastern, central and southern Europe
(Hoffmann 1957, Pinchuk et al. 2008) and more frequently in Kenya (Pearson 1974). Thus, the literature
and our own data show that a few adult Wood
Sandpipers might begin primary moult before migration or at a stopover area, and suspend or interrupt
their moult after arrival to move between wetlands, but
in southern Africa this is an infrequently used strategy.
Control of the rate of moult
One of the assumptions that underpins the Underhill &
Zucchini (1988) moult model is that the moult index
increases uniformly. The rate of primary feather mass
production in Wood Sandpipers was constant (Fig. 5),
confirming that this assumption held true for Wood
Sandpipers, as has been found in waders such as
Turnstone (Summers et al. 1989) and Purple Sandpiper
(Summers et al. 2004), but not in Redshank Tringa
totanus (Underhill et al. 1990) and Grey Plover (Serra &
Underhill 2006). The rate of primary feather growth in
the Grey Plover is regulated by the number of primaries
grown at a time and their inter-shedding intervals
(Serra & Underhill 2006). We found a similar mechanism in the Wood Sandpiper. The relative masses of the
three smallest primaries (P1–P3) that are grown almost
simultaneously (Table 3, Fig. 3) equal the mass of the
largest primary (P10) (Table 1). The larger the primary
being replaced, the fewer feathers were grown simultaneously (Fig. 4) and the longer the intervals between
shedding consecutive feathers (Fig. 3). As a result,
Wood Sandpipers maintained a constant rate of primary
feather mass production throughout moult (Fig. 5).
The effect of the wing gap
In Wood Sandpipers, the size of the gap in the wing
caused by moulting feathers, as described by PFMM,
decreased during the season as the PFMG increased.
This contrasts with the relationship described in Kelp
Gulls Larus dominicanus vetula moulting in South
Africa (Ward et al. in press), though both species have
similar relative masses for consecutive primaries, typical of waders and gulls (Underhill & Summers 1993,
Underhill & Joubert 1995). In the Wood Sandpiper, the
decrease in PFMM over the season is a consequence of
the initial intensive moult of up to five primaries, followed by a reduction in the number of larger feathers
ARDEA 97(3), 2009
that grow simultaneously (Fig. 4). The Kelp Gull moults
up to three primaries at all stages of its moult (Ward et
al. in press). The wing gap caused by shedding primaries increases the energetic costs of flight and impedes
bird’s ability to escape predators, but this can partly be
compensated for by the moulting birds keeping a lower
body mass (Slagsvold & Dale 1996, Hedenström &
Sunada 1999). The wing gap in the Wood Sandpiper
was on average only 10% of the mass of all primaries,
and adults maintain a low body mass between August
and February (authors’ unpubl. data), thus they retain
adequate flight ability to move between wetlands during moult.
Moult patterns among wader species
The duration of primary moult in the Wood Sandpiper,
estimated at 131 days, is longer than that estimated with
the Underhill & Zucchini (1988) model for populations
of Knot, Sanderling and Ruddy Turnstone moulting in
southern Africa, which complete moult in 95–119 days
(Underhill 2003). It is similar to those of the Curlew
Sandpiper Calidris ferruginea and the larger Grey Plover
(Fig. 7), which complete moult in 129 and 131 days
respectively (Serra 2002, Y. Barshep pers. comm.).
Prater (1981) suggested that at similar geographical latitudes waders with longer wings have longer primary moult durations. We therefore assembled from
the literature wing length and moult duration data for
southern Africa (Fig. 7). The durations of moult of
Wood Sandpiper, Knot, Sanderling, Curlew Sandpiper,
Ruddy Turnstone and Grey Plover were estimated using
the Underhill & Zucchini (1988) method. We also
included data on moult duration obtained from moult
curves ‘fitted-by-eye’ for Little Stint Calidris minuta
(Dean 1977) and Common Sandpiper Actitis hypoleucos
(Tree 2008). We estimated the moult duration of
female Ruffs Philomachus pugnax (Schmitt & Whitehouse 1976, their Table 4). For these nine species, the
correlation between wing length and primary moult
duration, i.e. Prater’s hypothesis, was not significant (r
= 0.43, n = 9, P = 0.13). We then split these species
into two groups: those exclusively using coastal habitats and those using inland habitats, allocating Curlew
Sandpiper to the inland group (Fig. 7). We fitted a
model with two parallel lines for the inland and coastal
groups (Fig. 7). This model explained 37.7% of the
variance in the duration of primary moult. The model
suggested that moult duration (days) for inland waders
was estimated from wing length w (mm) as 58.0 +
0.501w and for coastal waders 22.1 + 0.501w. The
model indicates that moult duration for inland waders
was 25.9 (SD = 12.2, t6= 2.12, P = 0.039, one-sided
160
moult duration (days)
278
140
Wood
Sandpiper*
Common
Sandpiper
120
Grey
Plover*
Curlew*
Sandpiper
Ruff
Ruddy
Turnstone*
*Sanderling
100
Little Stint
*Knot
coastal
inland
80
80
100
120
140
160
180
200
220
mean wing length (mm)
Figure 7. Relationship between wing length and moult duration
in waders at coastal and inland habitats of southern Africa,
located at similar geographical latitudes as the studied Wood
Sandpipers (see Fig. 1). Asterisks indicate that moult durations
were estimated using the Underhill & Zucchini (1988) model;
the remaining durations were obtained using ‘fitting-by-eye’
methods specified in original papers. Data sources for each
species are in the text. Unless specified in original study, wing
lengths are from Hockey et al. (2005). See text for explanation
of the regression lines for inland and coastal waders.
test) days longer than for coastal waders. Prater’s
(1981) hypothesis was confirmed, in that the slope
coefficient of 0.501 (SD = 0.197, t6= 2.55, P = 0.022,
one-sided test) indicates that, for each additional millimetre of wing length, the duration of primary moult
was extended by half a day. However, this modelling
was performed on small samples and needs further
confirmation. This is probably caused by the unpredictable and varied food resources and irregular nature
of inland habitats (Piersma 2003) that require species
using them to minimize gaps in primary feathers, so
that they are continuously prepared to undertake
nomadic movements. The Wood Sandpiper’s prolonged
moult is thus likely to be an adaptation to its almost
exclusive use of inland wetlands on migration and at
staging destinations (Cramp & Simmons 1983,
Underhill et al. 1997).
The moult of Wood Sandpipers has a different pattern to that of smaller and similar-sized coastal waders
moulting in southern Africa at similar geographical latitudes (Underhill 2003, Fig. 7). Knots, Sanderlings and
Ruddy Turnstones moult the inner primaries P1–P5 rapidly, up to four feathers simultaneously, with short
inter-shedding intervals (mean four days in all three
species) (Underhill 2003). Wood Sandpipers also grow
up to five inner primaries simultaneously, but with
longer inter-shedding intervals (mean seven days).
During the moult of P6–P10 the shedding intervals in
279
Remisiewicz et al.: MOULT OF WOOD SANDPIPERS IN SOUTHERN AFRICA
Wood Sandpiper were on average longer (mean 15
days) than in these three species (means 11–14 days;
Underhill 2003). The duration of the moult of corresponding primaries in Wood Sandpipers was longer
than for Sanderlings, Knots and Ruddy Turnstones, but
similar or shorter than those of Grey Plover (Underhill
2003, Table 3, Fig. 3).
The habitats that migrant waders choose in the
non-breeding season affect various population attributes, in consequence of their different life histories.
This paper supports the hypothesis that moult, which is
an important component of the migration strategy, is
another feature that differs between waders which use
coastal habitats and those that use inland wetlands. We
suggest that Wood Sandpipers have several adaptations
in consequence of their exclusive use of irregular and
ephemeral inland wetlands that provide variable and
unpredictable food resources: the small wing gap during moult, the prolonged moult duration achieved by
the slow growth of primaries, the long inter-shedding
intervals, and the extended period between the end of
primary moult and their departure to the breeding
grounds. Whether these adaptations are common to
other inland wader species needs confirmation.
ACKNOWLEDGEMENTS
This study was made possible through research grants to MR,
AG and LGU from the National Research Foundation (NRF),
South Africa, and the University of Gdańsk, Poland, within the
Poland-South Africa Agreement in Science and Technology. MR
was supported by a fellowship from the Claude Leon
Foundation. LGU acknowledges support from the SeaChange
Programme of the NRF. Lorenzo Serra, Danny Rogers, Ken
Rogers, Phil Battley, Guy Morrison, Peter Pyle and Joel Avni
commented on earlier versions of the manuscript; Joel Avni
assisted with language correction and editing.
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SAMENVATTING
In dit artikel worden de resultaten beschreven van een onderzoek naar de rui van de grote slagpennen van in zuidelijk
Afrika overwinterende Bosruiters Tringa glareola. Om de gevonden patronen in een breder kader te plaatsen, zijn ook de ruipatronen van andere in zuidelijk Afrika overwinterende steltlopers bij het onderzoek betrokken. De onderzoekers verwachtten dat Bosruiters als steltlopers van het zoete water een ruipatroon hebben dat lijkt op dat van andere steltlopers van het
zoete water en dat dit ruipatroon verschilt van dat van kustgebonden steltlopersoorten. Hiermee testten ze een onderdeel
van de hypothese van Piersma (2003) over contrasten tussen
vogelsoorten die in zoete en zoute habitats voorkomen. Om de
rui te beschrijven werden de ruiscores van de grote slagpennen
van 1496 volwassen Bosruiters gebruikt die in Zimbabwe en
Zuid-Afrika waren gevangen. Een deel van de ruiscores werd
bepaald aan museumexemplaren die waren verzameld in
Zimbabwe en Botswana. Start en duur van de rui werd zowel
voor de slagpennen afzonderlijk als voor alle tien slagpennen
gezamenlijk bepaald. Ook werd de ruisnelheid berekend van 16
Bosruiters die binnen hetzelfde seizoen waren teruggevangen.
Daarnaast werd geschat hoeveel veermateriaal er steeds werd
aangelegd. Volwassen Bosruiters arriveren in zuidelijk Afrika
tussen eind juli en november en vertrekken tussen half maart en
april naar de noordelijke broedgebieden. Bijna alle Bosruiters
ruiden alle grote slagpennen in zuidelijk Afrika. Slechts bij 56
vogels (7,5%) werd een onderbroken rui vastgesteld. De gemiddelde startdatum van de rui was 21 augustus, de gemiddelde einddatum 30 december. Daarmee komt de totale ruiperiode
op 131 dagen. Voor de terugvangsten was de gemiddelde periode 130 dagen. De hoeveelheid aangelegd veermateriaal was
uniform gedurende de ruiperiode, een gevolg van het feit dat
aan het begin de vijf binnenste, kortere, slagpennen gelijktijdig
groeien en aan het eind van de buitenste, langere, slagpennen
er maar een of twee tegelijk worden vervangen. De rui van de
grote slagpennen van volwassen Bosruiters (en andere binnenlandse steltlopersoorten) duurt langer dan de rui van steltlopersoorten van vergelijkbare grootte die in de kustgebieden
overwinteren. Maar doordat Bosruiters vroeg beginnen te ruien
zijn ze eerder klaar met de rui. Bosruiters hebben een tragere rui
omdat de tijdsperiode tussen het verliezen van de opeenvolgende slagpennen groter is en omdat de groei van de afzonderlijk pennen langer duurde. De auteurs veronderstellen dat de
langere duur van de slagpenrui en het ruim voor de terugtrek
beëindigen ervan aanpassingen zijn aan het gebruik van zoetwatergebieden. Het voedselaanbod van zoetwatergebieden in
zuidelijke Afrika is erg onvoorspelbaar en vereist dat de vogels
zich vaak moeten verplaatsen tussen snel veranderende binnenlandse ‘wetlands’.
(YIV)
Corresponding editor: Yvonne I. Verkuil
Received 21 February 2009; accepted 19 June 2009