The kinematics of feeding and drinking in palaeognathous birds in relation to cranial morphology
Institute of Biology Leiden, Evolutionary Morphology, Leiden University, Kaiserstraat 63, NL-2311 GP Leiden, The Netherlands
* Author for correspondence at present address: Division of Anatomy and Physiology, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The Netherlands (e-mail: s.w.s.gussekloo{at}vet.uu.nl)
Accepted 29 June 2005
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Summary |
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Key words: feeding behaviour, palaeognathae, cranial morphology, adaptation, Rhea americana
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Introduction |
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In the present study we did a functional analysis of the feeding behaviour
of the greater rhea Rhea americana (L.) in order to elucidate the
function and origin of the palaeognathous PPC. Several hypotheses can be
postulated about the evolution of the special PPC morphology in the
Palaeognathae. Our main hypothesis is that the specific palaeognathous
morphology of the PPC is an adaptation to selective forces that act on the PPC
in palaeognathous birds, but not in neognathous birds. Since the function of
the PPC is the transfer of forces and movements during upper bill movement, it
is assumed that these selective forces must be related to bill movement.
Feeding behaviour is considered the strongest selection force acting on bill
movement, and therefore on the PPC. Other behaviours such as vocalisation,
preening and social behaviour are considered to have little effect on the
osteology of the bills. To investigate whether differences in selection forces
on bill movement are present, bill movement of a typical palaeognathous bird
during feeding will be described and compared with a previously described
general neognathous-feeding pattern
(Zweers et al., 1994). If
differences are found in the feeding behaviour it may be possible to infer
which selective forces resulted in the differences in PPC morphology. If no
differences in feeding pattern can be found between Neognathae and
Palaeognathae it must be concluded that no different selective forces act on
the PPC during feeding and an alternative hypothesis about the origin of the
difference in morphology between Neognathae and Palaeognathae must be
postulated.
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Materials and methods |
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The feeding behaviour of the birds was recorded using video imaging (25
frames s1). The recordings were made in an experimental
set-up in which a lateral view and a frontal view of the bird were obtained in
the same frame using a mirror situated in front of the bird at an angle of
45°. The birds had to approach the feeding arena through a small corridor,
ensuring a good lateral position of the bird with respect to the camera.
Behind the bird, from the camera's viewpoint, a grid (2 cmx2 cm squares)
was placed to make scaling possible. The films were analysed, frame-by-frame,
by digitising the position of several points on the upper and lower bill
relative to the standard grid (Fig.
2). Prior to the feeding analysis the position of the bending
zones was determined through manipulating osteological specimens. The
positions found were compared to previous descriptions
(Hofer, 1954;
Simonetta, 1960
;
Bock, 1963
;
Zusi, 1984
) and used to
determine the position of points for digitising. In addition to these points
on the bills, some reference points on the skull of the bird were also
digitised (Fig. 2). From the
complete set of digitised points a number of distances and angles was
calculated (Table 1). The
accuracy of the calculated distances and angles was determined on the basis of
the variation in a standard measurement calculated as the distance between two
digitised points of the reference grid. The standard error in this distance
measurement was approximately 0.08 mm. The standard error in digitising a
point was therefore approximately 0.04 mm in each direction. The errors for
points were used to calculate the error for angles, which was dependent on the
distance between the points and the angle between lines. The standard error of
the mean angle of two parallel lines both of 4 cm (a typical length used in
our analyses) is just under 0.5°. For each time point the mean value and
95% confidence intervals of the behavioural parameters were calculated and
used to describe the mean behavioural pattern. The same data were also used to
test if cranial kinesis is present in palaeognathous birds.
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The data on head displacement were used to determine maximum velocities and accelerations of the head during feeding. The complete trajectory of the head was determined by interpolation to 250 points s1 using a cubic-spline interpolation technique. The spline interpolation technique was used under the assumption that head movements follow a gradual and symmetric path around the points of change of direction. Behavioural observations confirm these assumptions. The acceleration data, in combination with the mass of the head (estimated from the head mass in other individuals) were used to determine the forces acting on the head.
A range of food types was offered (Table 2), varying in size between 4 mm and 35 mm in length. At least five items of each food type were analysed for each bird. Large apples were only eaten by the male and only on three occasions. Drinking cycles were observed in both individuals, but only seven cycles could be analysed.
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To investigate the diversity and variability of the feeding behaviour, a Principal Component Analysis (PCA) was used to describe the variation in feeding behaviour due to different food-types. The PCA, with Varimax rotation, was based on the correlation matrix of characters. The characters were obtained from the movement patterns of the different head elements involved in feeding (Table 3; see also Figs 5, 6). Differences in principal component scores were determined using an analysis of variance (ANOVA).
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In addition to an analysis of the structure of the general feeding and drinking pattern, emphasis was laid on the presence of cranial kinesis, since many authors have coupled the morphology of the palaeognathous PPC directly to it. During all the observed feeding cycles both movement near the nasalfrontal area and movement in the upper bill were monitored to determine if cranial kinesis is present during normal feeding behaviour. Changes in angles were compared statistically using ANOVA to determine if bending actually occurs.
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Results |
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The general feeding sequence of the rhea (Figs 3A, 4) resembles this pattern: the bird approaches the food item while opening the bills and the food item is picked up. When the head hits the ground the acceleration of the head is approximately 11.30 m s2 (a=11.30±6.57 m s2, N=41). With an estimated head mass of 0.25 kg, the mean calculated impact force was 2.83 N and the maximum did not exceed 7.54 N (amax=30.17 m s2).
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When the food item was correctly positioned, a single `Catch and Throw' movement is used to transport the food particle into, or near to, the entrance of the oesophagus. A `Catch and Throw' movement starts when the food is fixed between the bills, the head is accelerated upward and slightly backward. Then the bills open and the head is suddenly moved forward. The accelerated food item continues to move upward while the head of the bird moves downward, which results in the transport of the food item. The palaeognathous single `Catch and Throw' movement is accompanied by a large gape and a large depression of the tongue. This depression results in an enlargement of the buccal cavity, which facilitates transport of the food item into the caudal part of the oropharynx. No tongue movement was observed other than the one resulting in the depression of the mouth floor. The limited functions of the tongue in feeding are reflected in the morphology of the tongue, which is relatively small with no remarkable features (Fig. 5). The oropharynx itself also shows very little remarkable characters that might indicate feeding patterns other than `Catch and Throw' behaviour.
General drinking behaviour
The rhea uses two different types of drinking behaviour, depending on the
area of water available to drink from. The preferred method of drinking can be
described as scoop drinking followed by a low-amplitude tip-up phase
(Fig. 3B). During drinking the
bird opens the bill, inserts it into the water, and with a forward scooping
motion of the head the lower bill is filled with water. The bill is then
closed and the head is elevated until the neck is almost completely stretched,
while the head itself is in a horizontal position. Finally, the water is
transported into the oesophagus by a slight elevation of the bill tips and a
retraction of the tongue. In some cases small horizontal `Catch and Throw'
movements are used to transport the water more caudally in the oropharynx just
prior to swallowing.
When the size of the water surface limits the scooping movement, the rhea uses a drinking technique that is very similar to pecking behaviour. The bill is opened and inserted almost vertically into the water, the bill is then closed and in a single head jerk the water is accelerated vertically, the bill is opened and the water is transported to the back of the oropharynx. Since this behaviour strongly resembles pecking, and is not the basic drinking behaviour, it was not included in this analysis.
Quantitative differences between food types
To characterise the movement patterns quantitatively 36 parameters were
chosen (Table 3, Figs
4,
6) and analysed using a
Principal Component Analysis (PCA). The first three principal components of
the PCA (PC13), based on the characters of the feeding and drinking
behaviours described 63% of the total variance. An analysis of variance
(ANOVA) over the principal component scores was used to determine the main
differences between individuals/sexes and food types. None of the first three
principal components showed a difference between individuals/sexes (d.f.=47,
PC1: F=0.264, P=NS; PC2: F=0.198, P=NS;
PC3: F=0.240, P=NS, where NS=not significant) and therefore
the data from both individuals were combined. It is clear from the plot of the
first principal component (PC1) against the second principal component (PC2)
that drinking behaviour is remarkably different from feeding behaviour
(Fig. 7, Table 4). The first principal
component describes the absence of the second gape movement (`Catch and Throw'
movement), differences in neck movement (duration of the neck cycle) and the
duration of the total feeding cycle (Table
5). The second principal component describes differences in food
manipulation by the bills, such as position of the food item between the
bills, depression of the lower bill and upper bill kinesis. To investigate the
differences between food types without the large distorting effect of
drinking, the PCA was repeated using the four types of feeding behaviour only.
In this analysis 65% of the variance was explained by the first three
principal components. To test whether there are significant differences
between food types, a one-way ANOVA over the first three principal components
scores was used. Differences between the food types were tested using a
t-test with Bonferroni correction. There are significant differences
between food types on both the first and third principal component (d.f.=40,
PC1: F=28.678, P<0.001; PC2: F=0.365,
P=NS; PC3: F=3.628, P<0.05). It is clear that
PC1 describes the effect of food size (Fig.
8). The differences on the first principal component represent
mainly the effect of the duration of the movement for each food type (e.g.
gape period, head elevation period, food period, lower bill period), the size
of the first gape (Gape 1) and the elevation of the head (difference head
Y; Table 6). All these
parameters increase with an increase of the size of the food type, which
indicates that the movement pattern of food uptake is relatively constant and
that only the duration, mainly the effect of repositioning, and amplitude of
the movement differ between different food sizes. The change in movement
described by PC1 becomes smaller when the size of the food items increases. A
difference on PC1 is only found between seeds and all other food types (food
type 1 vs 2, 3 and 4, t-test, Bonferroni correction,
P<0.001).
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The third principal component mainly describes the handling of the food item, which affects the amount of depression of the lower bill (lower bill at Gape 1), position of the food item between the bills during the upward movement of the head (food level, food level S.D.), and amplitude of cranial kinesis (e.g. prokinesis at Gape 1 and 2, rhynchokinesis at Gape 2; Table 6). Differences between food types on PC3 are only found between large apples and seeds (food type 1 vs 4, t-test, Bonferroni correction, P<0.05). However, no clear trends can be determined with a change in size of the food types.
Cranial kinesis
To test the presence of kinesis in the skull of the rhea, several
measurements were taken. The movement between the cranium and the upper bill
around the point where the nasalfrontal hinge would be in prokinetic
birds was measured, and will be further referred to as prokinetic movement
(Fig. 1A). A second measure of
kinesis was the movement between the rostral and caudal part of the upper bill
with the border of the two parts in the bending region of the upper bill.
Movement of the rostral part relative to the caudal part of the upper bill
will be referred to as the rhynchokinetic movement
(Fig. 1B). Since food types are
different in size, the kinesis of the upper bill was determined for each food
type separately. The large apple was not used for this analysis due to the
small number of repeated measurements.
It is assumed that maximal kinesis is observed during the large amplitude gapes when the food item is picked up or swallowed. Velocities of the head are very large during the second phase of the `Catch and Throw' movement, which makes it very difficult to determine points accurately. Because of this low accuracy and the relatively small movements in the upper bill, cranial kinesis could only be analysed accurately in the grasping phase. From repeated experiments the average pick-up cycle was calculated and plotted with the standard error. The plot of gape vs time shows a clear pattern (Fig. 9A) similar to a single food uptake cycle, and differences between the time segments are significant (ANOVA, small apple: d.f.=85, P<0.001; pellets: d.f.=90, P<0.001; seeds: d.f.=168, P<0.001; water: P<0.001).
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Angular measurements were also used to test the response of prokinetic and rhynchokinetic movement during the feeding cycle. Prokinetic movement showed a pattern similar to the lower bill movement but with a much smaller amplitude (Fig. 9B). However, the prokinetic movement pattern is not significant for any food type or drinking (ANOVA; small apple, d.f.=87, P=NS; pellets: d.f.=89, P=NS, seeds: d.f.=167, P=NS; water: d.f.=102, P=NS). The rhynchokinetic movement patterns can be clearly recognised except in the drinking behaviour (Fig. 9C), but are only significant for the two largest food types, small apple and pellets (ANOVA, small apple: d.f.=84, P<0.05; pellets: d.f.=88, P<0.05; seeds: d.f.=166, P=NS; water: d.f.=98, P=NS). In Table 7 the maximal changes in the mean angles of the different types of kinesis are given, showing an increase in cranial kinesis with an increase in food size.
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Discussion |
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Similarly, the drinking behaviour of the rhea lacks the tongue movement
present in neognathous drinking. The general drinking pattern of neognathous
birds (Zweers, 1992) consists
of (1) a fixation phase, in which the bird orientates its head, (2) the
downstroke, in which the head is lowered towards the water, (3) the immersion
phase, during which the actual water intake takes place, and (4) the upstroke,
in which the head is positioned in such a way that gravitational forces
facilitate transport of the water from the oropharynx into the oesophagus
(swallowing). All these phases are also represented in palaeognathous drinking
behaviour and similar to neognathous phases. Large differences, however, are
found in the immersion phase. In the rhea there is no stationary immersion
phase but a scooping motion, the bill remains widely opened, and no tongue
movement is observed during this phase. Intra-oral transport during immersion
in Neognathes always includes pro- and retraction of the tongue. Only during
the head upstroke does a single protraction of the tongue in rhea facilitate
the movement of the water into the oesophagus.
Although feeding and drinking behaviours were analysed under controlled
conditions, field data show that the observed feeding behaviours are present
in the natural behaviour of the rhea as well. The natural feeding and
food-acquisition behaviour of all Palaeognathae, except the kiwi
(Apteryx sp.), can be described as browsing, which means eating a
wide variety of plant material with some occasional carnivorous food. The food
preferences of the greater rhea in the wild
(Martella et al., 1996)
suggest that no fundamentally different feeding behaviours are required, other
than the ones analysed in our study. The diet consists of a wide variety of
food items, but is mainly vegetarian
(Mosa, 1993
;
Martella et al., 1996
;
Quin, 1996
). The assumption
that the feeding behaviour is characteristic for all Palaeognathae is confimed
by a number of observations. The single `Catch and Throw' feeding behaviour
and both the scooping and `Catch and Throw' drinking behaviour have been
observed in the greater rhea in the wild. We also observed the single `Catch
and Throw' feeding behaviour in wild and captive ostriches Struthio
camelus L., captive emus Dromaius novaehollandiae Latham and
captive cassowaries Casuarius casuarius (L.). Although there are some
differences between the diets of the various palaeognathous species, these
seem due to local food availability, and not to preference or performance.
In order to determine the importance of cranial kinesis in the feeding
behaviour of the palaeognathous species, we determined bending both in the
area of the nasalfrontal articulation and in the upper bill itself. Our
study showed that during feeding behaviour kinesis is found between the
rostral and caudal part of the upper bill in rhea. No, or only very limited,
bending occurs in the area of the nasalfrontal articulation, the
position where in many neognathous species the nasofrontal hinge is
situated. The elevation amplitude of the bill tip relative to the cranium in
the rhea is similar to the elevation of the upper bill found in prokinetic
neognathous birds (approximately 510°;
Kooloos and Zweers, 1989;
Heidweiller and Zweers, 1990
;
van den Heuvel, 1992
).
One hypothesis about the role of rhynchokinesis states that it reinforces
the grip on food items by simultaneously depressing the upper bill tip and
elevating the lower bill tip, as found in certain Charadriiformes
(Zusi, 1984). No upper bill
depression is observed in the rhea, which indicates that rhynchokenesis is not
used in this way in Palaeognathae.
Our video recordings of beak movement suggested that there may be a
difference between neognathous rhynchokinesis and paleognathous
rhynchokinesis. While a clear bending point is present in Neognathae, the
upper beak in rhea seems flexible over its full length. The elevation angle of
the upper bill gradually declines more caudally in the upper bill. This
strongly suggests that a single hinge or narrow bending zone is not present in
Palaeognathae. This conforms with the description of Zusi
(1984), who named this
flexibility over the full-length `central' rhynchokinesis. The relation
between rhynchokinesis and the detailed anatomy of the beak is explored in an
accompanying paper (Gussekloo and Bout,
2005
).
Phylogenetic analysis of feeding behaviour
To determine whether the feeding behaviour of the Palaeognathae is derived
or primitive within modern birds, a comparison can be made with the general
feeding patterns found in other tetrapods. The method of feeding in tetrapods
depends on the presence of a well-developed lingual apparatus. If a
well-developed lingual apparatus is absent two main types of non-lingual
feeding are present within the tetrapods: inertial feeding and the feeding
pattern observed in snakes (de Vree and
Gans, 1994). Comparison of the feeding behaviour of the rhea with
the nearest living sister group of birds, the crocodilians, shows that the
feeding behaviour of the rhea is more similar to reptilian inertial feeding
than the general feeding pattern of neognathous birds
(Zweers et al., 1994
;
Cleuren and de Vree, 1992
). In
crocodilian intra-oral transport the tongue elevates the food item until it
presses against the palate. Then gape is rapidly increased and the cranium
moved forward (the avian `Catch and Throw'), while the tongue is depressed to
enlarge the buccal cavity and to facilitate the transport of the food item. In
the rhea the final transport of a food item into the oesophagus is achieved by
a retraction of the hyolingual apparatus
(Tomlinson, 2000
), similar to
transport in crocodilians. The fact that feeding behaviour of the rhea
resembles feeding behaviour of crocodilians, and lacks certain elements found
in the general feeding pattern of neognathous birds, seems to suggest that
inertial feeding behaviour is basal within birds. This would agree with the
widely accepted hypothesis that the Palaeognathae are the oldest offshoot in
the phylogeny of modern birds (Bock,
1963
; Meise, 1963
;
Parkes and Clark, 1966
;
Cracraft, 1974
;
de Boer, 1980
;
Prager and Wilson, 1980
;
Sibley and Ahlquist, 1981
;
McGowan, 1984
;
Feduccia, 1985
;
Handford and Mares, 1985
;
Elzanowski, 1986; Houde, 1986
;
Bledsoe, 1988
;
Caspers et al., 1994
;
Lee et al., 1997
;
van Tuinen et al., 1998
;
Simon et al., 2004
). However,
lingual feeding is found in the more primitive amphibians
(de Vree and Gans, 1994
), and
present in many reptilians (Bramble and
Wake, 1985
; Reilly and Lauder,
1990
; Herrel et al.,
1996
). As crocodiles are a very distant sister group of birds the
possibility remains that crocodiles and Paleaognathae are specialized inertial
feeders and that lingual feeding is the most primitive avian feeding
mechanism. Tetrapod inertial feeding is believed to have evolved many times
independently within vertebrates (de Vree
and Gans, 1994
). The simple movement patterns of the tongue in
rhea may be the consequence of a reduction in size related to efficient `Catch
and Throw' feeding behaviour. Since it cannot unambiguously be determined
whether the feeding pattern of the palaeognathous birds is primitive or a
specific adaptation, these data cannot be used to determine the phylogenetic
position of the Palaeognathae.
General discussion
From the comparison of feeding patterns we conclude that the feeding and
drinking behaviours of the rhea resemble those of neognaths, but lack certain
elements found in the general feeding pattern of neognathous birds, especially
with respect to tongue movements. We found no elements in the feeding
behaviour that might impose additional functional demands on the PPC, nor are
any of the behavioural elements investigated more demanding than in
neognathous feeding. This indicates that the specific morphology of the PPC is
not the result of specific functional demands from palaeognathous feeding
behaviour. Also the hypothesised role of rhynchokinesis in relation to the
cranial morphology could not be confirmed. Central rhynchokinesis is present
in the upper bill, but does not play an important role in improving grip on
the food item or in increasing the gape. It must therefore be concluded that
the kinetic feature of the bill is not the factor that determined the
morphology of the PPC.
Alternative explanations for the presence of the characteristic PPC complex
have been suggested. Bock
(1963) proposed that the
special morphology of the PPC might be an adaptation to the high impact forces
on the bill during pecking. Our movement analysis showed that the rhea is
capable of controlling the impact force of pecking. The head hits the ground
at approximately 11.30 m s2. The mean calculated impact
force was 2.83 N and the maximum did not exceed 7.54 N. Using a compressive
strength of 170x106 Pa for bone we can calculate that a
cross-sectional area of the bones of just 0.05 mm2 is sufficient to
withstand these forces. It seems clear that this area is many times smaller
than the actual cross-sectional area in the skull of the rhea.
Another explanation is that the morphology of the palaeognathous PPC is the
result of selection forces that are not directly related to feeding, but do
affect the morphology of the PPC indirectly. While Paleognathae are often
believed to be basal to Neognathae, an alternative hypothesis states that
Palaeognathae have actually a derived phylogenetic position and have evolved
through neoteny from a flying ancestor (de
Beer, 1956). The hypothesis on the neotenous origin of the
Palaeognathae was recently revived by physiological/ontogenetic data
(Dawson et al., 1994
) and
molecular systematics (Mindell et al.,
1997
; Härlid and Arnason,
1999
). The physiological/ontogenetic experiments showed that
induced neoteny in neognathous birds results in a morphology of the PPC that
was similar to that of the Palaeognathae, while the molecular systematic data
show a derived position of the Palaeognathae within the Neognathae and not a
basal position of the group. A comparison of the cranial morphology of the
Palaeognathae with different developmental stages of neognatous birds showed,
however, that not a single developmental stage resembles the palaeognathous
configuration (Gussekloo and Bout,
2002
). This is a clear indication that the palaeognathous PPC is
not the result of neoteny.
A third hypothesis on the origin of the special morphology of the
palaeognathous PPC proposes that the morphology of the extant palaeognathous
PPC is the result of the continuous reduction of bony and ligamentous elements
in the lateral aspect of the skull
(Gussekloo and Zweers, 1999).
Although birds in general have less bony and ligamentous elements in the
lateral aspect of the skull than closely related groups such as dinosaurs and
other reptiles, Palaeognathae have even less than most birds. Compared to
Neognathae, Palaeognathae lack a clear Ligamentum postorbitale and
the lateral bar of the upper bill (Bock,
1964
; Zusi, 1984
).
The reduction of these elements might have resulted in a relatively unstable
configuration of the upper bill, especially under conditions of external
loading. The only type of food acquisition that is not covered by our study is
pulling leaves off plants. It is possible that this way of feeding imposes
special functional demands on the construction of the upper beak. The removal
of leaves is mainly achieved by neck motion, and generates external forces on
the upper bill. While preliminary observations showed that the transport of
the food items used in the present study is very similar to the transport of
grass or leaves that are removed from the plant, it is possible that the
morphology of the upper bill of the Palaeognathae is adapted to oppose the
reaction forces during pulling (see also
Gussekloo and Bout, 2005
).
Although it seems that such a force regime is not unique for Paleognathae
(e.g. grazing geese, pulling off berries by passerines), it is unique when
combined with the absence of lateral bars in the skull. Since the
Palaeognathae could not counteract the external forces by reinforcing these
lateral elements, it may have been necessary to reinforce the unstable upper
bill configuration in the ventral elements, resulting in a more rigid PPC. As
a consequence of this reinforcement of the ventral plane of the upper bill,
active kinesis of the upper bill may also become limited. Additional
experiments to test this hypothesis are described in the accompanying paper
(Gussekloo and Bout,
2005
).
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