Captive Red Knots (Calidris canutus) fed soft food pellets developed atrophied stomachs, and were reluctant to eat their usual hard-shelled mollusc prey. An interspecific comparison among shorebirds showed that wild Red Knots and other intact-mollusc-eating species have gizzards with relatively great mass but very small proventriculi. Within six different shorebird species, the heavier individuals usually had the heavier stomachs as well, but in Red Knots and Bar-tailed Godwits (Limosa lapponica) we identified heavy premigrant individuals with reduced stomach masses, suggesting a reallocation of protein reserves before long-distance flights. In both species reduced stomach mass was associated with a relatively soft diet. We were unable to show that during adjustment of stomachs to hard-shelled prey, such prey are broken down to smaller fragments. We attribute this to the counteractive influence of the pylorus during adjustment. We summarize the suggested stomach/diet interactions as a network of causal relationships and feedback loops involving the type of diet and gizzard mass. We identify two basic modifiers of gizzard mass: one working via endurance training and disuse atrophy; and another involving endocrine and/or neural mechanisms. It is likely that, in the course of their annual cycle, shorebirds are prevented from achieving maximal digestive performance owing to seasonal changes in feeding habitats and diet enforced by their long-distance migrations. Received 28 May 1992, accepted 25 November 1992.
Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands; and
Zoological Laboratory, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands
ANIMAL BODIES are dynamic systems showing
large changes in composition in relation to sea-
son, nutritional condition and diet (e.g. Allison
and Wannemacher 1965, King 1972, Goldberg
et al. 1974, 1975, Raveling 1979, Cherel et al.
1988, Blem 1990, Gaunt et al. 1990). Variation
in the form and mass of stomachs in relation to
diet has long attracted the attention of research-
ers (e.g. Darwin 1885; summary in Ziswiler and
Farher 1972), and a series of detailed studies
indicates that associations between stomach mass
and type of diet often represent species- and
individual-specific adaptations (Table 1). For
example, eating more fibrous food usually leads
to increased gizzard mass (i.e. the muscular part
of stomach), as has been shown in experimental
as well as in observational studies. Having a
particular stomach morphology because of ex-
posure to a particular diet might constrain the
ingestion rate, or the digestive yield, of other
food types (Moss 1983), at least during the pe-
riod in which the stomach is adjusting.
Although fiber-eating wildfowl and galli-
forms are widely recognized as birds with large
and muscular stomachs, species with similar
stomach types that feed on hard-shelled animal
prey ingested whole have escaped detailed at-
tention; only casual remarks on mollusc-eating
sea ducks have been made (Bellrose 1976, Barnes
and Thomas 1987, Brown and Frederickson
1987). Some shorebird species, such as Red Knots
(Calidris canutus), also feed on whole bivalves
and gastropods, which they capture by probing
in soft intertidal sediments (Prater 1972, Goss-
Custard et al. 1977, Boere and Smit 1980b, Piers-
ma 1991, Zwarts and Blomert 1992).
During experimental studies on the feeding
behavior of Common Eiders (Somateria mollis-
sima; P. Duiven and C. Swennen pers. comm.)
and Red Knots, we repeatedly have found that
individuals conditioned to soft food pellets did
not eat their natural hard-shelled prey for a
couple of days. Such observations, and those on
Wild Turkeys (Meleagris gallopavo) and Surf-
birds (Aphriza virgata) listed in Table 1, further
suggested that gizzard mass may influence diet
rather than vice versa. Because most shorebirds
show considerable seasonal variation in the
types of habitat frequented (e.g. marine inter-
tidal in winter, tundra in summer), and because
these shifts coincide with changes in prey type
(e.g. hard-shelled molluscs in winter, soft ar-
thropods in summer), we examined the rela-
tionship between diet and gizzard morphology
in this group of birds.
We first describe some behavioral observa-
tions on captive Red Knots that led us to asso-
ciate diet with stomach mass in shorebirds, both
TABLE 1. Diversity of suggested interactions between diet and stomach mass in birds as documented in
modern studies. Mass of the stomach, or its muscular part (gizzard) only, is usually interpreted as measure
of strength.
Refer-
Type d Predator(s) Food type Nature of diet/stomach interaction ence b
Wild Turkey (Meleagris Hickory nuts
gallopavo)
B Surfbird (Aphriza virgata) Two mussel species
(Mytilidae)
I Wildfowl (Anatidae) Invertebrate and
plant food
I Lorikeets (Psitticacidae) Nectar/pollen vs.
seeds / fruits
S Spruce Grouse (Canachites Leaves and conifer
canadensis ) needles
S Bearded Tits (Panurus Insects vs. seeds
biarmicus )
S Ducks (Anas) Invertebrates and
plant material
S Geese (Anseridae) Plant material
S Phainopepla (Phainopepla Berries
nitens)
E Crow/domestic chick Mixed plant/animal
(Corvus/Gallus) food vs. meat
E Mallard (Anas platyrhyn- Corn, variety of
chos) food pellets
Domestic birds used to soft food (less pow- 1
erful stomach?) refuse to eat hard-shelled
nuts
Selection for the mussel species that re- 2
quires least force to break
Herbivores and omnivotes have heavier 3, 4
gizzards than carnivores eating fiber-free
food
Species eating soft nectar/pollen have less 5
muscular gizzards than other parrots
Heaviest gizzard when eating fibrous food 6
(conifer needles in midwinter)
Gizzards in summer (insect diet) weigh 7
only one-half of winter ones (seed diet)
Gizzards are heaviest in periods of the 8-12
most fibrous (plant) diet
Gizzard mass correlated with daily intake 13-15
Change from bulk to single berry feeding 16
coincides with reduction of gizzard by
50%
Birds fed pure meat develop small stom- 17, 18
achs (only 36% of reference mass)
Fibrous diets lead to heavy gizzards 19, 20
"Nature of study: (B) behavioral observations; (I) interspecific comparisons; (S) seasonal changes detected in population; (E) experimentally
induced changes.
References: (1) Schorger 1960; (2) Navarro et al. 1989; (3) Kehoe and Ankney 1985; (4) Barnes and Thomas 1987; (5) Richardson and Wooller
1990; (6) Pendergast and Boag 1973; (7) Spitzer 1972; (8) DuBowy 1985; (9) Heitraeyer 1988; (10) Whyte and Bolen 1985; (11) Paulus 1982; (12)
Drobney 1984; (13) Ankney 1977; (14) I-Ialse 1985; (15) Hobaugh 1985; (16) Walsberg and Thompson 1990; (17) Oelhafen-Gandolla and Ziswiler
1981; (18) Lenkeit 1934; (19) Kehoe et al. 1988; (20) Miller 1975.
intra- and interspecifically. Although heavier
birds of a species usually have heavier stom-
achs, we describe three cases in free-living Red
Knots and Bar-tailed Godwits (Limosa lapponica)
in which obese premigrant individuals have the
lightest stomachs and contained the softest prey.
This observation led to an experiment with Red
Knots to show the value of a conditioned and,
presumably, heavy and strong stomach.
Our central question is whether the large sea-
sonal changes in habitat and diet of shorebirds
(e.g. Lange 1968) temporarily constrain the use
and, thereby, the intake of certain prey (cf. Di-
amond and Obst 1988). Most shorebirds are long-
distance migrants with tight annual schedules
and a great capacity to store and use tissues
rapidly (e.g. Drent and Piersma 1990, Evans and
Davidson 1990, Piersma and Jukema 1990, Gud-
mundsson et al. 1991). The muscular stomach
might be one of the body components that such
migrants can adaptively exploit as a nutrient
source (and perhaps even as a nutrient sink).
METHODS
Feeding experiments.--Flocks of 3 to 10 Red Knots
were kept in outdoor cages measuring 2.0 by 3.5 m
with a height of 2 m. Feeding trials were conducted
with individual knots in small cages (0.5 x 0.5 x 0.5
m) in climate rooms at constant temperatures (1.5 ø,
19.0 ø or 33.0 to obtain a range in daily food re-
quirements) and with a 13-h daylight period. Fresh-
water was always available. In addition, small flocks
of foraging birds were studied on an artificial outdoor
tidal flat measuring 7 x 7 m. Normally, our captive
birds were fed protein-rich, trout-food pellets. In ex-
perimental situations we also offered them four bi-
valve and one gastropod prey, namely the edible mus-
sel (Mytilus edulis), edible cockle (Cerastoderma edule),
Balthic tellin (Macoma balthica), and mudsnail (Hy-
drobia ulvae) from the intertidal flats, and the subtidal
bivalve Spisula subtruncata. The bivalves were collect-
ed at a variety of localities near the island of Texel
(The Netherlands).
A series of feeding trials was carried out specifically
to establish whether a longer exposure to hard-shelled
molluscs leads to a stomach with greater muscle mass.
The characteristics of the food (length distribution,
length-dependent shell mass and biomass) ingested
during a 24-h experimental period were described in
detail (see Dekinga and Piersma 1993). Each feeding
trial started at 1300 MET with food being placed in
the cage. The following morning (at 0900) the re-
maining food was taken away, leaving the birds 4 h
in which to empty their guts before the experiment
ended at 1300. The feces were collected, dried to con-
stant mass at 55 ø to 60øC, weighed, and then sieved
through 2-mm, 1-mm, 630-/m, 500-/m, 400-/m, 315-
/m, 200-/m and 100-/m mesh sieves. Median feces-
fragment size was calculated by plotting on proba-
bility paper the cumulative mass retained on the in-
creasingly larger-meshed sieves. We then determined
median fragment size at 50% mass. A score for prior
experience was calculated as the sum of the relative
hardness of the prey ingested during the seven days
before the experiment (highest for Hydrobia, lowest
for food pellets; see below) times a weighting factor
for recency (a factor of 7 for day before experiment,
6 for penultimate day, etc.).
Breaking forces required.--A few seconds after ex-
perimental Red Knots had ingested bivalve prey, and
usually before another prey was taken, we could hear
the shell being cracked in the stomach. This suggested
that breaking shells between two flat surfaces might
provide a reasonable simulation of the cracking pro-
cess. The force required to crack mollusc prey of vari-
able sizes was measured by slowly increasing the
pressure at a constant rate on freshly collected live
specimens mounted between a flat metal plate and a
flat wooden plate on an electronic balance. The max-
imum exerted weight (in kg) needed to break the shell
was taken as the measure of force (in Newtons, kg/
10).
Diet and body composition of wild shorebirds.--Details
on the body composition of a large number of shore-
bird carcasses were accumulated from 1979 to 1991.
All birds were accidentally killed during catching
operations, by flying against lighthouses, or during
mass-starvation incidents during severe winter
weather periods in north temperate wintering areas.
The sample included individuals originating from the
wintering and staging areas in west Africa (see Ker-
sten and Piersma 1983, Piersma and van Brederode
1990, Zwarts et al. 1990), southeastern and north-
western Australia (Piersma and Barter 1991), The
Netherlands (Goede et al. 1990, Piersma and Jukema
1990), Germany, Great Britain (Summers et al. 1992),
and Iceland (Gudmundsson et al. 1991). After a vari-
able period (up to four years) of storage in deep freez-
ers, carcasses were weighed (though, when possible,
body mass at death was used) and dissected. The com-
plete stomach was excised, its contents removed, and
the fresh mass taken. The carcasses then were dried
to constant mass at 55 ø to 60øC and the fat extracted
in a Soxhlet apparatus, using petroleum ether (boiling
traject 40ø-60øC) as the solvent.
Throughout this paper "stomach mass" refers to the
sum of the mass of the proventriculus (glandular an-
terior part of stomach) and the mass of the gizzard
(muscular posterior part). Note that all sandpipers
and plovers examined had small proventriculi rela-
tive to their gizzards. We weighed proventriculi and
gizzards separately in two Red-necked Stints (Calidris
ruficollis) and two Red Knots, and found that the pro~
ventriculus contributed an average of 6.3% to stomach
mass (range 4.3-8.6%). Of the species examined, only
the Eurasian Oystercatcher (Haematopus ostralegus) had
a well-developed glandular stomach, as the proven-
triculus contributed, on average, 28.0% to stomach
mass (range 24.1-31.5%, n = 3).
Stomach contents were stored in 90% ethanol for
later examination. Reconstructions of the spring diet
of Red Knots from Mauritania and Bar-tailed Godwits
from The Netherlands were made on the basis of
preserved samples. We used published (Zwarts 1988,
Zwarts and Esselink 1989, Dekinga and Piersma 1993)
and unpublished (L. Zwarts pers. comm., Piersma pers.
observ.) sources to estimate the proportional com-
position in terms of wet mass.
RESULTS
How hard are hard-shelled prey?--In all four
mollusc species examined, breaking force scaled
to shell length with an exponent of about 3 (Fig.
1), indicating that breaking force scales linearly
to shell mass. This confirms the findings of Cur-
rey (1979) and Vermeij and Currey (1980). Na-
varro et al. (1989), however, found breaking
force to scale with the much lower exponents
of 1.53 to 1.70 on shell length in two mussel
species.
During the feeding trials, Red Knots ingested
tiny Hydrobia snails or small Mytilus (up to 15
mm long), Cerastoderma (up to 12 ram) or Ma-
coma (up to 16 ram). The size ranges taken rel-
ative to the required breaking forces of the dif-
ferent species (Fig. 1) imply that their gizzards
had to generate forces similar to those exerted
by us between two flat plates (i.e. up to 0.4 N).
Within the size ranges of prey taken, we ranked
Hydrobia as the hardest prey to crack, with My-
tilus, Cerastoderma, Macoma and pellets being
successively easier.
Knots used to soft food dislike hard-shelled prey.-
Captive Red Knots took several days to adjust
to a novel food type, especially if it was a hard-
shelled bivalve such as Spisula (Table 2). Red
Knots always immediately began feeding on
familiar (and soft) food pellets and required
about a day before starting to feed on familiar
shellfish, such as Mytilus (Table 2). Why are
1.,4
1.2
2 4 6 8 10 12 14 16 18 20 22 24 26
shell length (mm)
Fig. 1. Scaling of force (F, in Newtons) required
to break mollusc prey of varying sizes and species on
shell length (SL, in mm). Only data points for Hy-
drobia ulvae (dots) and Macoma balthica (squares) shown
in addition to calculated regression lines for these
two species plus Cerastoderma edule and Mytilus edulis.
Relevant details of log-log regression equations are
for: Hydrobia, F = 0.001979SL2% r 2 = 0.73, n = 29;
Macoma. F = 0.000018SL 3'"27, ? = 0.86, n = 32; Ceras-
toderma, F = 0.000101SL 2994, r = 0.89, n = 37; Mytilus,
F = 0.000446SL3% r = 0.96, n = 50.
captive, but clearly hungry, birds reluctant to
feed on their natural hard-shelled prey?
Figure 2 shows that free-living Red Knots,
even if they have starved to death in midwinter,
have heavier stomachs than captive birds (cf.
Moss 1972). The average wet masses of the stom-
ach and the body of well fed and starved birds
from the wild were respectively (œ _+ SD): stom-
ach, well fed, 8.8 _+ 2.3 (n = 67); stomach,
starved, 7.2 _+ 1.5 (n = 5); body, well fed, 141.1
_+ 26.1; body, starved, 87.9 _+ 3.3 g. Stomach and
TABLE 2. Time delay (œ _+ SD) in accepting a new
food type by Red Knots kept in captivity. Differ-
ences between time delays before accepting a soft
after a hard food type and the reverse treatment
are significant, both when new food is novel as
when it is not (Student's t-test, P < 0.05). Daily
energy requirements during these experiments were
similar, since experiments were carried out in en-
closed cages at air temperatures between 15 ø and
25øC.
Type of change Delay in days n"
Pellets to Spisula 4.5 + 1.7 4
Molluscs' to pellets ø 1.1 _+ 0.4 8
Pellets to Mytilus 2.0 _+ 0.6 5
Mytilus to pellets 0.0 25
Spisula to pellets 0.0 4
"Number of individual diet changes in which delays were properly
recorded.
"Probable novel food type.
ß "Molluscs" refers to unspecified mollusc prey taken in field before
exposure to food pellets in captivity
WILD KNOTS
20 :;"we, fed :-..
starved ....
lO
> CAPTIVE KNOTS
. n:10
20
10
fresh mass of stomach (g)
Fig. 2. Red Knots in wild (top) have much heavier
stomachs than those in captivity (bottom), even if
former have starved to death in severe weather in
winter. Inset in bottom panel shows typical examples
of gizzards (cross-sectioned through thickest part of
muscle wall) of a 130-g wild (top) and a 125-g captive
(bottom) Red Knot.
body masses in the sample of 10 captive birds
averaged 3.5 + 0.7 g and 109.0 _+ 10.0 g, re-
spectively. The change in stomach mass in cap-
tivity is expressed in a large decrease in the
cross-sectional area of the gizzard of captives
fed only with soft food pellets (Fig. 2 inset).
The captives' apparent reluctance to eat hard-
shelled prey, along with their small stomach
mass, suggests that wild birds have stomachs
that are adjusted to crack hard-shelled molluscs
with heavy muscular gizzards. Given these
findings, we asked whether wild Red Knots have
heavy stomachs in comparison with other
shorebird species, including those with softer
diets.
Allometry of stomach mass in shorebirds.--An
analysis of a sample of 135 stomachs of five
species (Greater Golden-Plover, Pluvialis apri-
caria; Red Knot; Red-necked Stint; Purple Sand-
piper, Calidris maritima; and Bar-tailed Godwit)
showed that the excised stomachs consisted of
T^BLE 3. Average wet masses (g + SD) of body and stomach (proventriculus + gizzard) in 19 species of
shorebirds (Charadrii). Includes only apparently healthy birds from nonbreeding season (usually inadver-
tently killed during catching operations).
Species n Body mass (g) Stomach mass (g)
! Eurasian Oystercatcher (Haernatopus ostralegus) 3 546.67 + 30.7! !5.60 + 0.54
2 Ringed Plover (Charadrius hiaticula) 6 53.40 + 8.2! 1.!8 + 0.25
3 Snowy Plover (C. alexandrinus) 2 4!.75 + 0.25 !.25 + 0.35
4 Greater Golden-Plover (Pluvialis apricaria) 80 2!7.85 + !9.!9 5.43 + !.!5
5 Black-bellied Plover (P. squatarola) 2 234.50 + 9.50 8.2! + 2.01
6 Great Knot (Calidris tenuirostris) 5 !95.86 + 36.99 9.34 + 2.98
7 Red Knot (C. canutus) 67 !4!.36 + 26.!3 8.82 + 2.25
8 Sanderling (C. alba) ! 56.00 !.80
9 Red-necked Stint (C. ruficollis) !57 26.93 + !.87 1.08 + 0.!8
!0 Little Stint (C. minuta) !4 26.0! + 3.52 0.74 + 0.!0
!! Curlew Sandpiper (C. ferruginea) ! 65.00 !.50
!2 Purple Sandpiper (C. rnaritirna) 6 65.63 + 5.2! 3.95 + 0.55
!3 Dunlin (C. alpina) 55 49.96 + 9.62 !.97 + 0.5!
!4 Black-tailed Godwit (Limosa limosa) 3 3!7.77 + 52.95 !0.4! + 0.4!
!5 Bar-tailed Godwit (L. lapponica) 84 320.30 + 69.52 8.98 + 3.06
!6 Whimbrel (Nurnenius phaeopus) 3 5!0.00 + 40.82 20.!3 + 4.28
!7 Eurasian Curlew (N. arquata) 3 870.83 + 72.28 35.95 + 4.47
!8 Redshank (Tringa totanus) 3 !54.33 + !6.0! 3.83 + !.38
!9 Ruddy Turnstone (Arenaria interpres) 6 !02.67 + 7.36 2.55 + 0.72
9.1 + 6.2% fat (range 0.0-29.6), 27.2 + 3.6% other
dry matter (15.5-43.1) and 63.7 + 6.0% water
(47.6-81.9). The percentage of fat of the wet
stomach mass was positively correlated with the
5O
A Oystercatcher
0 Plovers
ß Scolopacids/Sandpipers
_c 5
t 12
o
10 50 100 500 1000
body mass (g)
Fig. 3. Allometry of stomach mass and body mass
in sample of !9 species of shorebirds of three families:
(!) oystercatchers (Haematopodidae; n = !, open
square); (2) plovers (Charadriidae; n = 4, open circles);
and sandpipers (Scolopacidae; n = !4, closed dots).
Allometric relationship for all 19 data points is Y =
0.0295X 02 (r 2 = 0.93). Equations for individual fam-
ilies: plovers, Y = 0.0!93X ø77 (r = 0.96); sandpipers
(including Ruddy Turnstone), Y = 0.03!!X ' ø29 (r 2 =
0.92). Numbers refer to species listed in Table 3.
fat index of the entire body (i.e. 100 [fat mass/
body mass]), with a linear regression of Y = 0.74
+ 0.64X (r 2 = 0.59, P < 0.05).
Stomach mass in shorebird species (data list-
ed in Table 3) is isometric with body mass (i.e.
an exponent of 1; see Fig. 3). The allometric
regressions yielded an exponent of 1.026 (not
significantly different from one) across all spe-
cies, with a slightly higher value for the sand-
pipers (1.066) than for plovers (1.029). A co-
variance analysis showed that neither the slopes
nor the intercepts differed significantly be-
tween sandpipers and plovers. However, some
sandpiper species had relatively heavy stom-
achs, with particularly high values being re-
corded in Red Knot (89% heavier than average),
Purple Sandpiper (84% heavier), and Great Knot
(44% heavier). The diet of these species consists
in large part of held-shelled molluscs which are
ingested whole (Cramp and Simmons 1983, Lane
1987, Summers et al. 1990), thus supporting the
suggested interspecific association between a
diet of shellfish and a heavy stomach.
Do the allometric relationships, with expo-
nents close to 1, also hold within species? In
the six species we examined, stomach mass was
positively correlated with body mass, though
the exponents varied widely from 0.28 in Red
Knots to 1.39 in Greater Golden-Plovers (Fig.
4). The low slopes in Red Knots and Bar-tailed
Godwits were due to a few particularly heavy
individuals with light stomachs (Fig. 4). These
0.1 LITTLE STINT RED KNOT .
o.o ß
-0.4
-0.5
slope = 0.52 slope = 0.28
-0.6 r 2 = 0.24 r 2 = 0.04
RED-NECKED STINT GOLDEN-PLOVER
slope = 1.00 slope = 1.39
r2=0.17 r2=0.48
0.4
0.2
" 0.0
-0.4
-0.6
1.2 _ ___ B_AR_-T_AILED GODWIT
DUNLIN ' . " ' "': '
2.5 ß
1.0 '" "
0.8 ß . ß ß 2.1 .,,"
ß '. .
0.6 1.7 ß. ; ß ß
0.2 ß slope =0.45 1.3 ' slope =0.80
ß ß r2=0.11 r2 =0.22
0.0 I I I I I I I . , , , 09 , i i i i i i i i i
3.1 3.3 3.5 3'.7 3.9 4.1 4.3 ' 4.4 4.6 4.8 5.0 5.2 5.4 5.6 5.8 6.0 6.2
In (body mass) (g)
Fig. 4. Allometry of stomach mass and body mass in Little Stint (n = 14), Red-necked Stint (n = 157),
Dunlin (n = 55), Red Knot (n = 72), Greater Golden-Plover (n = 85), and Bar-tailed Godwit (n = 84). Sample
sizes are slightly bigger than those in Table 3 because information for starved wild birds also included here.
All regression coefficients significantly different from zero at 5% level.
heavy birds contained large fat loads (pets. ob-
serv.) and were sampled shortly before depar-
ture on a long-distance migration to the arctic
breeding grounds (Piersma and Jukema 1990).
This observation raises the question whether
stomach masses change in relation to the mi-
gratory cycle.
Stomach mass and long-distance migration.--Red
Knots of the subspecies islandica winter in Eu-
rope and breed in the High Arctic of Greenland
and Canada (Davidson and Wilson 1992; for re-
view of subspecies, see Piersma and Davidson
1992). They are represented by an early spring
sample (March) from Dutch and German parts
of the Wadden Sea, and a sample from late May
of birds ready to leave from Iceland (see Gud-
mundsson et al. 1991). Birds staging in the Wad-
den Sea in early spring had a significantly great-
er stomach mass than individuals just before
their departure to the arctic breeding grounds
captured later in spring in Iceland (Fig. 5, top),
even though the former group had a much low-
er body mass (135 + 13 g) than the latter (208
+ 11 g). A decreasing stomach mass during the
period of premigratory body-mass gain was also
evident in Red Knots of the subspecies canutus
14
12
10
8
ß Calidns canutus islandica
0 Calidris canutus canutus
5
14 Limosa lap_ponica
ß stomach mass
E 0 stomach index
,- 12 26
10
8
6 g
4
2 2 8
EARLY -25 -20 -15 -10 -5 0
;PRING
days before departure on
long-distance flight
Fig. 5. Decreases in stomach mass prior to long-
distance migration in two populations of Red Knot
(top) and in Bar-tailed Godwits (bottom). Averages
with 95% confidence intervals and sample sizes are
shown. Analyses of variance indicated that between-
sample variation to be larger than the within-sample
variation in all three examined cases (islandica Knots,
F = 32.2, P < 0.001; canutus Knots, F = 11.4, P = 0.001;
Bar-tailed Godwits, stomach mass, F = 4.4, P = 0.016;
Bar-tailed Godwits, stomach index, F = 3.93, P = 0.025).
(migrating between West Africa and Siberia; see
Piersma et al. 1992) on the Banc d'Arguin, Mau-
ritania (Fig. 5, top).
The Bar-tailed Godwits staging in May in The
Netherlands are of a population migrating from
the West African wintering grounds to the Si-
berian breeding areas (see Drent and Piersma
1990, Piersma and Jukema 1990,1993). A similar
pattern as in Red Knots was detected in the
stomach masses of staging Bar-tailed Godwits
(Fig. 5, bottom). Having arrived after a 4,300-
km flight (ca. 25 days before next departure),
the birds had depleted their nutrient reserves
(Piersma and Jukema 1990, Lindstr6m and
Piersma 1993), which apparently also negative-
ly affected their stomach mass. As a conse-
quence of the initially depleted state, the pat-
tern is best reflected by the changes in stomach
index (100[stomach mass/body mass]). During
the staging period when body mass increased
(with both fat and proteins being stored; Lind-
str6m and Piersma 1993), relative stomach mass
decreased.
In the Red Knots from Mauritania the pre-
departure decrease in stomach mass was asso-
ciated with a decrease in the incidence of hard-
shelled prey remains in the stomachs. There
were on average, respectively, 46 + 10, 29 _+
20 and 14 _+ 12 mollusc fragments in the stom-
achs of the three successive groups of birds de-
picted in Figure 5.
Diet and stomach structure in Bar-tailed God-
wits.--Bar-tailed Godwits have a particularly
variable diet in the Wadden Sea during spring
staging. They feed both on hard-shelled mol-
luscs and on soft-bodied polychaete worms
(Boere and Smit 1980a), and on insect larvae
and lumbricid worms in the adjacent fields (pers.
observ.). Is the highly variable diet of Bar-tailed
Godwits also associated with stomach mass (Fig.
5, below), as in the Red Knots from Mauritania?
Of the 55 analyzed stomachs of Bar-tailed
Godwits, 16 contained leatherjackets only. Of
the 14 godwits with the remains of soft-bodied
polychaete worms (Nereis diversicolor) only one
also contained leatherjackets, whereas of the 25
godwit stomachs with the remains of marine
molluscs (usually Macoma balthica), 12 con-
tained leatherjackets too. The proportion of Ne-
reis-eating birds additionally containing leath-
erjackets is significantly smaller than the
proportion of mollusc eaters (X 2 = 10.1, df = 1,
P < 0.01). Leatherjackets have no hard parts but,
as their common name implies, they are rather
strong-skinned. Their well preserved state in
the stomach indicates that they are hard to wear
down. The diet of the godwits, therefore, con-
sisted either of: (1) soft and easily digested prey
(Nereis); or (2) hard-shelled (Macoma) and/or
tough-skinned (leatherjacket) prey.
Godwits feeding on soft prey were heavier
but had lighter stomachs than those feeding on
other prey types, and their stomachs contained
fewer stones but more grit (Table 4). The high
average body mass of Nereis eaters indicates the
presence of heavy premigrant godwits in the
sample, but is also due to a higher percentage
TABLE 4. Body, stomach and relative stomach masses
(œ + SD) and their dry-grit content in Bar-tailed
Godwits containing either hard-shelled molluscs
and leatherjackets (tipulid larvae), or soft-bodied
polychaete worms (Nereis diversicolor) as prey re-
mains. Birds were accidentally collected in May
1984-1989 on their spring staging area in the Dutch
Wadden Sea.
Prey category
Molluscs and/
or leather-
jackets Nereis
Variable (n = 41) (n = 14) t-value a
Body mass (g) 314.7 + 56.7 392.9 + 91.0 3.02**
Stomach mass
(g) 10.0 + 3.1 7.5 + 1.9 3.62***
Stomach in-
dex b (%) 3.2 + 0.8 2.3 + 0.6 4.16'**
Stones (grit)(g) 1.0 + 1.08 0.3 + 0.3 3.40***
Shell grit (g) 0.1 + 0.2 0.4 + 0.4 2.37*
"Indicates whether values of two categories differ significantly from
zero (two-sided Student's t-tests). *, P < 0.05; **, P < 0.01; ***, P <
0.005.
100(stomach mass/body mass).
of females (the larger sex) in the Nereis-eating
sample (57%) than in the mollusc/leatherjacket
sample (27%). The significantly smaller stomach
index of the category of birds feeding on soft
prey, nevertheless, indicates an association be-
tween stomach mass and diet in migrant Bar-
tailed Godwits. Relatively heavy stomachs oc-
curred in birds feeding either on hard-shelled
prey or on tough-skinned prey that require the
grinding action of stones for proper digestion.
Light stomachs were found in birds feeding on
worms.
Do trained stomachs crack better?--Why do birds
feeding on hard-shelled prey have heavier
stomachs? Do large stomachs crack better, or
would lighter stomachs become exhausted too
soon when they have to deal with large num-
bers of hard-shelled prey? On the assumption
that a better cracking performance by the stom-
ach would reveal itself in the droppings in shells
fragmented to smaller pieces, the hypothesis
that trained and heavy stomachs crack better
was tested by examining median fecal-fragment
size produced by Red Knots fed on a particular
prey type with different recent diet experienc-
es. We assumed that training effects would be
evident within a week (Goldberg et al. 1975,
Piersma 1988, Mufti and Qureshi 1989). The at-
tempt to correlate fecal-fragment size of birds
fed with Mytilus and Hydrobia against a score
for prior experience was complicated because
TABLE 5. Results of two stepwise multiple regres-
sions to estimate median fragment size in feces in
which prey size (shell length, SL), daily intake (dry
mass ingested during a 24-h experimental period,
DI) and prior experience (hardness score weighted
for number of days before, PE) are consecutively
entered as independent variables.
Multiple-regression parameters
Standard-
Independent ized coef-
variable ficient (/) T-value P-value
Mytilus (n = 58) a
Shell length 0.50 5.47 <0.001
Daily intake 0.34 3.00 0.004
Prior experience 0.24 2.16 0.035
Hydrobia (n = 16) b
Shell length 0.11 0.33 0.746
Daily intake 0.22 0.79 0.445
Prior experience 0.18 0.55 0.594
Equation: Y = 44.9SL + 3.IDI + 2.6PE + 49.9 (r = 0.55, P < 0.05).
No equation (r = 0.12, P > 0.05).
several variables other than recent prior expe-
rience with hard-shelled prey appeared to be
highly correlated with fecal-fragment size. Birds
eating larger Mytilus produced larger fecal frag-
ments as did birds eating more Mytilus (Table
5). Taking these two effects into account statis-
tically, we came to the surprising conclusion
that conditioned birds produced larger fecal
fragments (Table 5). The results for Hydrobia,
although not statistically significant, were sim-
ilar. We, thus, must reject our hypothesis that
trained stomachs lead to more fragmented prey
remains.
DISCUSSION
Pyloric complications.--The pylorus is the
structure that determines how long food items
remain in the stomach and are subject to its
forces. The pyloric region is the muscular com-
plex around the exit from the stomach to the
small intestine. The pylorus ensures that only
properly degraded particles enter the intestine
(Stevens 1988). It is likely that the pylorus be-
comes increasingly "relaxed" and allows hard
particles to enter the intestine sooner upon pro-
longed exposure to hard shell fragments (see
Levey and Duke 1992). Because retention and,
therefore, fragmentation times in the gizzard
will become shorter, increasingly large frag-
ments would be found in the feces. A strong
modifying effect of the pylorus on stomach re-
DAILY
(ENERGY)
INTAKE
PHOTO-
PERIOD /
CIRCANNUAL
OSC LLATOR
GIZZARD
MASS
I MIGRATORY I REALLOCATION
NUTRIENT 1> OF PROTEIN
DEMANDS STORES
Fig. 6. Scheme outlining a set of hypotheses about feedback loops between food type and gizzard mass,
and about points of interaction of other identified influences on gizzard mass, based on our findings for
shorebirds and those reported for other species (see Table 1 and text).
tention times, and a change in its "admission
criteria," would account for the observed de-
creases in median mussel-fragment size upon
exposure to a hard-shelled diet. The only dis-
advantage of passing large shell fragments is
potential tissue damage to the intestines. If both
pylorus and intestines can adjust to passing
larger fragments the birds may benefit because
the processing rate would increase.
The low apparent assimilation efficiency (39%)
of horseshoe crab (Limulus polyphemus) eggs in-
gested by Sanderlings is a consequence of the
majority of eggs passing through the digestive
tract intact (Castro et al. 1989). It is likely that
the small egg diameter (1 mm) allows horseshoe
crab eggs to pass rapidly through the pylorus,
thereby foregoing grinding by the gizzard.
Shorebirds consuming horseshoe crab eggs in
Delaware Bay during spring migration (Myers
1986) might benefit from a pyloric filter system,
such as the pyloric feather plug of grebes (Pod-
icipedidae; Piersma and van Eerden 1989).
Diet/stomach interactions.--Shorebirds appear
to exhibit almost all the relationships between
stomach mass/structure and diet that are known
in other birds (Table 1): (1) experimental ex-
posure to soft food leads to light gizzards; (2)
individuals with atrophied gizzards initially re-
fuse to ingest hard-shelled prey; (3) shorebird
species that feed on molluscs have relatively
the heaviest stomachs; (4) light and thin-walled
stomachs are associated with diets of soft prey.
The indication that Red Knots and Bar-tailed
Godwits show stomach atrophy during general
body hypertrophy before long-distance flights
is parallelled by a similar observation of an un-
accountable decrease in stomach mass of pre-
migratory fattening Greater Snow Geese (Chen
caerulescens atlanticus; Gauthier et al. 1984); in
the case of the geese, there was no change in
diet.
The diet/stomach relationship is dynamic and
reciprocal. On the basis of the literature sum-
marized in Table 1 and our own findings, we
have tried to integrate the (causal) interactions
that may be involved in Figure 6. The crux of
the problem of whether gizzard mass influences
diet is the position of the valve in the upper
right corner, allowing a fully hard-shelled or
fiber-rich diet, or not. Assuming that it is the
gizzard part of the stomach that critically influ-
ences diet choice, we suggest that the mass of
this organ is influenced by direct (endurance)
training and by atrophy through disuse (caused
by changes in ingested volume or characteris-
tics of prey), as well as through the effects of
endocrine or neural modifiers. The latter mech-
anism may be involved in a possible realloca-
tion of protein reserves prior to long-distance
flights, as in Bar-tailed Godwits. A direct en-
docrine or neural mechanism was also implied
by Spitzer (1972) in his study of the dramatic
changes in stomach structure and mass of
Bearded Tits (Panurus biarmicus), changes that
occurred independently of migratory events.
Spitzer suggested that a photosensitive circan-
nual oscillator caused the seasonal changes in
stomach mass, which in turn were associated
with changes from seed to invertebrate diets.
Two different diet types apparently lead to
heavy muscular stomachs, and they involve two
different functional requirements. Tough-
skinned prey (such as leatherjackets) and fiber-
rich food probably require long gizzard reten-
tion times during which the food is ground and
worn down, usually with the help of stones (see
studies of herbivores summarized in Table 1,
and Table 4). Hard-shelled prey, which can be
cracked singly or against each other instead of
being ground slowly with the help of grit, re-
quire a strong muscular gizzard as well, but
probably involve much shorter stomach reten-
tion times. Such a dichotomy in diet and reten-
tion times in birds with muscular stomachs
might suggest correlated differences in the rel-
ative contribution of the stomach to the chem-
ical breakdown of food. Since no chemical ac-
tion can be carried out in the proventriculus
where prey are intact, and since little digestive
work can occur during the short stage in the
muscular gizzard, we suggest that the intestines
of birds feeding on hard-shelled prey play a
larger role in digestion than they do in either
birds feeding on fiber-rich food, in which part
of the chemical breakdown is carried out in the
stomach, or in birds feeding on soft food, in
which the glandular stomach begins the process
of the chemical breakdown. Alternatively, the
meat contained in hard-shelled prey might gen-
erally be so easy to digest that "lack of stomach
digestion" and "ease of digestion" could cancel
each other out.
A number of issues remain. Does a long-term
exposure in the field to soft food always lead
to reduced gizzard mass? It may fail to do so if
endocrine/neural modifiers interfere (Fig. 6).
Does the presence of a weak gizzard constrain
the dietary options, and for how long? The only,
admittedly weak, evidence that gizzards do
temporarily constrain diets is supplied by the
fact that Bar-tailed Godwits with light stomachs
and worm diets were particularly prominent
among fat premigratory females, in spite of the
fact that Nereis worms are abundantly available
on the feeding grounds all through the godwits'
staging period (Zwarts 1988); Nereis might not
be the preferred prey and is only taken when
stomach structure prevents a focus on hard or
tough prey.
The time course of such constraints was not
resolved, but clinical studies of muscle hyper-
trophy show rapid effects of training, with over
one-half of the muscle usually being built up
within a week (Goldberg et al. 1975, Mufti and
Qureshi 1989). The significance of this finding
is that, if a summer season on the tundra with
a diet of relatively soft terrestrial invertebrates
results in reduced stomach mass in arctic-breed-
ing shorebirds, we might expect them to require
time to adjust to a diet of hard-shelled mollusc
prey on their return to the nonbreeding
grounds. If shorebirds try to maximize the speed
of migration (Alerstam and Lindstr/Sm 1990,
Gudmundsson et al. 1991) and if periods of only
one week matter (Piersma 1987), the diet/stom-
ach interaction described here may have con-
siderable relevance to birds in the wild. Indeed,
this was recently implicated by Klaassen and
Biebach (in press) in their study of fattening
and starvation in migrant Garden Warblers (Syl-
via borin). After a period of starvation, which
mimicked the use of nutrient reserves during a
long-distance flight, Garden Warblers had sub-
maximal intake rates for several days, which the
authors attributed to limitations imposed by a
reduced digestive tract. The increase in staging
time for refattening induced by suboptimal
feeding contrasts with the rest of the metabolic
adaptations of Garden Warblers, which can all
be interpreted as being designed to speed up
migration.
Diet-, activity-, or season-induced changes in
the digestive tract, thus, may affect a host of
behavioral and ecological phenomena dis-
played by birds. Further study will undoubt-
edly yield more quantitative insight into the
ways in which the digestive physiology of birds
constrains their behavioral performance.
ACKNOWLEDGMENTS
Part of the experimenta! data presented here were
collected in feeding experiments carried out by Jef-
frey Samuels and Jan van Gils. Throughout we were
stimulated by the feedback of fellow wader and ben-
thos workers on Texel and in Groningen, and we
thank Cees Swennen, Piet Duiven, Jan Beukema, Ger-
hard Cade, Jaap van der Meer, Mardik Leopold, Leo
Zwarts, Rudi Drent, Marcel Kersten, Anne-Marie
Blomert, Jan van der Kamp, Popko Wiersma, Jan van
Gils, Niels Cade, Martin Poot, Ingrid Tulp, Petra de
Goeij and Cherry Ott for this support. Jan Hegeman
kindly re-invented the (almost) "universal testing
machine" to measure breaking forces on shells. Mem-
bers of the Dutch wader expeditions to western Af-
rica, and Joop Jukema, Piet Zegers, Lida Goede, Georg
Nehls, Hans-Ulrich R6sner, Gudmundur Gudmunds-
son, Ron Summers, Belinda Gillies, Danny Rogers and
Mark Barter were instrumental in making available
the shorebird carcasses for analyses. Ben Helming and
Rients Hofstra of the van Hall-Instituut in Groningen
arranged that A.K. and A.D. could participate as part
of their study. The illustrations were drawn by Dick
Visser. John Goss-Custard, Sue Jackson and Joe Jehl
carefully edited the first draft, while we also grate-
fully acknowledge the constructive comments made
by Hugh Boyd, G. E. Duke, Nick Davidson, Henk
Visser, Jan Beukema, Leo Zwarts, Gerhard Cade, ref-
erees, and the Editor.
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