Cranial kinesis in palaeognathous birds
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, NL-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: cranial kinesis, palaeognathae, cranial morphology, adaptation, external force
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Introduction |
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Most birds are able to move the upper bill as a whole, a situation known as
prokinesis (Fig. 1A;
Bock, 1964). In prokinetic
birds the bending zone between the skull and the moveable upper bill is
situated at the nasalfrontal hinge. Other bending zones are situated on
the transition between the palate and the upper bill and between the jugal bar
and the upper bill. The prokinetic upper bill itself contains no flexible
zones and is rigid. This type of cranial kinesis is considered the most basic
form within modern birds (Neognathae; Bock,
1964
). Several other types of cranial kinesis can be
distinguished, based on different positions of the bending zones
(Fig. 1). After prokinesis the
second most common type is the rhynchokinetic configuration
(Zusi, 1984
). In this type the
bending zones are positioned further rostrally, within the upper bill.
Therefore only a small portion of the upper bill is moveable, and no flexible
zone is present near the nasalfrontal connection. In the rhynchokinetic
configuration clear bending zones are present in both the dorsal and ventral
bars of the upper bill (Fig.
1B).
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Although the main division in types of cranial kinesis is between
prokinetic and rhynchokinetic skulls, a number of sub-divisions are recognized
within the rhynchokinetic skulls, which are characterized by different
positions of the flexible zones in the dorsal and ventral bar
(Zusi, 1984). In most of these
types of rhynchokinetic skulls a schizorhinal nostril is present, except in
central rhynchokinesis in which a holorhinal nostril is found, which has a
configuration similar to that of the nostril in the prokinetic morphology. In
this type of skulls uncoupling of the dorsal and ventral bar is achieved by a
reduction of the lateral bar, resulting in a ligamentous part in the lateral
bar of the upper bill (Fig.
1C). Bühler
(1981
) has described the
bending zones in the central rhynchokinetic configuration to be long and
located near the center of the upper bill. This description of the bending
zones in central rhynchokinesis is endorsed by Zusi
(1984
), but it is unclear how
the position of these bending zones was determined. It is remarkable that this
type of rhynchokinesis is described for one avian taxon only: the
Palaeognathae. Central rhynchokinesis is therefore also referred to as
palaeognathous rhynchokinesis. The conclusion that palaeognathous birds might
be rhynchokinetic has been drawn mainly from analyses of skull only. Recently,
however, behavioural data showed that bending actually occurs in the upper
bill of the Palaeognathae during feeding. The data also showed that bending
occurs in a large area, confirming the description of central rhynchokinesis
(Gussekloo and Bout,
2005
).
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In birds in general the PPC, in combination with the quadrate, has a clear
function in the movement of the upper bill. The movement of the upper bill is
caused by a forward rotation of the quadrate, which is transferred to the
upper bill via the PPC (Bock,
1964; Gussekloo et al.,
2001
). It has always been assumed that the PPC in the
Palaeognathae serves the same function, but that a specialised morphology of
the PPC is required for effective central rhynchokinesis
(Bock, 1963
;
Hofer, 1954
;
Simonetta, 1960
). Recently it
has been shown that the movement patterns of the neognathous and
palaeognathous PPC are comparable
(Gussekloo et al., 2001
). This
contradicts the hypothesis that there is a functional relationship between the
type of cranial kinesis and the specific morphology of the palaeognathous
palate. Without a clear relationship between the morphology of the PPC and
central rhynchokinesis the origin of the palaeognathous PPC might be
completely different.
Several advantages of a kinetic skull have been suggested (see
Zusi, 1993), including higher
biting forces (Zweers et al.,
1997
) and higher closing speeds
(Herrel et al., 2000
).
However, the functional interpretation of cranial kinesis in birds is still
problematic and a general explanation might not hold. While for some taxa,
such as the Charadriiformes, the type of cranial kinesis is linked to specific
ways of feeding (Zusi, 1984
;
Kooloos et al., 1989
;
Zweers and Gerritsen, 1997
),
cranial kinesis may be an inherent feature of the design of the skull in
others (Bout and Zweers, 2001
;
Herrel et al., 2000
). At
present the exact role of cranial kinesis in the feeding behaviour of the
Palaeognathae is unknown, although it is clear that it does not have the same
function as in Charadriiformes, which use rhynchokinesis to catch prey that is
buried in the substrate (Gussekloo and
Bout, 2005
).
Since it seems that there is no direct connection between the palaeognathous PPC and rhynchokinesis, we must consider other options with respect to the origin of the specific morphology of the palaeognathous PPC. When looking at bending in the upper bill there are two options: the upper bill may either bend intentionally by applying muscle force (as in Charadriiformes), or the upper bill can bend as a result of external forces when picking up food items. In living animals these external forces might be counteracted by muscle force, but this will not be noticed when only looking at osteological specimens. In that case a non-rigid configuration may be falsely identified as adapted to induced rhynchokinesis.
To determine whether the skull of the Palaeognathae is truly adapted to
induced (active) rhynchokinesis we test whether the morphology of the skulls
of the Palaeognathae fits the requirements for effective rhynchokinesis on the
basis of a number of characters found in known rhynchokinetic birds, such as
Charadriiformes (Zusi, 1984;
Gerritsen, 1988
). The specific
characters of known rhynchokinetic species are: (1) the presence of an
uncoupling of the movement of the dorsal and ventral bar, (2) the presence of
clear bending zones in both the ventral and dorsal bar of the upper bill, and
(3) a configuration of muscles and bony elements in the skull that results in
sufficient force output to open the upper bill. The uncoupling of the dorsal
and ventral bar in the Palaeognathae is achieved by a ligamentous part in the
lateral bar and has been described before
(Fig. 1C; Bock,
1963
,
1964
;
Zusi, 1984
). Therefore we only
address the presence of bending zones and analyses of forces.
To test the alternative hypothesis in which the palaeognathae possess an upper bill morphology that is intrinsically flexible and actively stabilised by muscle force, we analysed the intrinsic resistance against bending during closing of the bill, and the amount of muscle force that can be used to stabilise the upper bill. By comparing the data we determined whether the Palaeognathae are truly rhynchokinetic or that the characters of the upper bill and PPC are the result of other factors, and try to elucidate the possible function of the specific upper bill configuration of the Palaeognathae.
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Materials and methods |
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Skull measurements
To test whether flexible zones are present in the upper bill of the
palaeognathous birds the thickness of the ventral and dorsal elements was
measured. The measurements were performed on both sides of the specimens used
for the force measurements. The thickness of both ventral bars and the dorsal
bar were measured using a digital calliper rule (Sylvac, Crissier,
Switzerland; accuracy 0.01 mm). One ostrich bill was used to make transverse
sections, which were stained according to the van Gieson technique
(Bradbury and Keith, 1990) and
used to measure the thickness of the dorsal and ventral bars more accurately
under a dissection microscope using a measuring eyepiece. For comparison, the
thickness of the dorsal and ventral bars were measured in a similar way in
transverse sections of the bills of the purple sandpiper Calidris
maritima (Brunnich) and the sanderling Calidris alba (Pallas),
which have a clear distal rhynchokinetic skull. All thickness measurements
were scaled to the head width, measured at the quadratojugal
articulation, to eliminate potential size differences between individuals.
Intrinsic force measurements of the upper bill
The forces necessary to elevate the upper bill were measured using a force
transducer (Aikoh, Osaka, Japan). The head was fixed with screws on each side,
and a bar was attached to the skull to prevent dorso-ventral rotation
(Fig. 3). The force transducer
was attached to the tip of the upper bill. For elevation a small hook was
attached to the upper bill and the force transducer was slowly moved upward by
a step motor. The force transducer moved with a speed of 5 mm
s1 while elevation force and distance were recorded
continuously. During the experiments the skull was videotaped from a lateral
viewpoint. These recordings were later used to determine the position of
maximal bending due to external forces. All experiments were performed at room
temperature.
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Model
The estimated maximal muscle forces were used to calculate the opening and
closing force that can be exerted on the upper bill, and the maximal biting
force. These forces were calculated using an adapted version of a
two-dimensional (2D) model of the avian jaw apparatus
(Bout and Zweers, 2001) and
included the skull represented as a four-bar system, the lower jaw
(Fig. 4) and the reaction force
at the processus basipterygoideus (Fig.
2). Such a 2D model follows accurately the three-dimensional
measured movement of skull elements in several types of avian cranial kinesis
(Gussekloo et al., 2001
). The
bars represented the quadrate, the PPC, the caudal side of the moveable part
of the upper bill, and the (stationary) skull between the rotation point of
the quadrate and the flexible zone in the dorsal bar of the upper bill. The
quadrate bar had the length and orientation of the quadrate. The PPC bar had
the length and the orientation of the line between the quadratojugal
articulation and the centre of the bending zone in the ventral bar of the
upper bill. The centre of the bending zone was determined from behavioural
analyses (Gussekloo and Bout,
2005
) in combination with the video recordings from the intrinsic
force measurements (see above). The bill-bar is defined by the line between
the centres of the bending zones in the ventral and dorsal bar. Finally, the
skull is described by the line between the quadrateskull articulation
and the centre of the bending zone in the dorsal bar of the upper bill. The
moveable part of the upper bill is represented by a triangle defined by the
bill-bar and the bill tip, and moves as a whole with the bill-bar. The
position of the rotation points of the model were determined as the centre of
the zone of maximal flexion in lateral radiograms of manually elevated upper
bills and in video recordings of the force measurement experiments. The
lengths of the elements of the four bar system were measured in lateral
radiograms. Orientations of muscles were estimated in lateral radiograms from
the known position of origo and insertio of the muscles. The lower jaw
articulates around the quadratomandibular articulation and is in its
rest position in all calculations, which is in agreement with the situation
when feeding on green plant material, comprising 90% of the natural diet of
the rhea (Martella et al.,
1996
). All forces were calculated assuming static equilibrium.
Several forces were calculated using the model. (1) The opening force of
the upper bill (Elev. UB), defined as the force at the bill tip (perpendicular
to the long axis of the beak) necessary to balance the maximal force of the
upper bill opener muscle (musculus protractor pterygoideus et quadrati). (2)
The closing force of the upper bill (Depr. UB), defined as the force at the
bill tip (perpendicular to the long axis of the beak) necessary to balance the
total muscle force generated by muscles depressing the upper bill only
(musculus pseudotemporalis profundus, musculus adductor mandibulae ossis
quadrati and musculus pterygoideus). This force was calculated with the bills
in rest position but also for an elevation of the upper bill of 10°. (3)
The maximal biting (jaw closing) force (Max. close) was calculated as the
maximal force acting on a food item of 0 mm (very thin) at the beak tip
(closing muscles of upper and lower bill combined). The first calculation is
an indication of the amount of muscle force that can be used to intentionally
elevate the upper bill, the second is an indication of the muscle force
available to counteract external forces that might elevate the upper bill, and
the third gives an indication of total biting force. The calculations also
included the reaction force of the processus basipterygoideus
(Fig. 2). This process is
absent in many other species, but has a characteristic morphology in
Palaeognathae (McDowell,
1948). It blocks caudal movement of the PPC when the PPC is in its
resting position. The combinations of muscle forces required for the maximal
jaw forces were found iteratively. Since no leftright asymmetries were
found in the natural feeding behaviour
(Gussekloo and Bout, 2005
),
all forces were calculated for a leftright symmetrical muscle force
pattern.
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Results |
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In rhynchokinetic birds with known functional bending zones, such as
Calidris, a clear bending zone can be recognised as an area of low
relative thickness in the rostral part of the dorsal and ventral bar (Figs
5,
6). These zones of reduced
thickness coincide accurately with the position of the bending zones as
determined from behavioural data
(Gerritsen, 1988; arrows in
Figs 5,
6) indicating a direct link
between the slender zones and bending.
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Intrinsic force measurements upper bill
The forces at the bill tip necessary to elevate the upper bill are
relatively small (Fig. 10).
Within the physiological elevation range (010°;
Gussekloo and Bout, 2005) the
forces increase almost linearly. The rhea and ostrich show similar resistance
to bending. From Fig. 10 it is
clear that the upper bill of the emu resists bending more than in the other
two species.
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When we consider the thickness of the ventral and dorsal bars of the upper bill of the different palaeognathous species (Figs 7, 8, 9), it is clear that the thickness of the dorsal bar is related to the measured bending forces. The emu has on average the thickest dorsal bar (Fig. 9) and the highest resisting forces to elevation (Fig. 10), while the ostrich and rhea have thinner bars, which require lower bending forces.
Opening and closing forces
Maximal opening and closing forces were calculated using a 2D static force
model, which uses estimated maximal muscle forces and the coordinates
describing the position of muscles and skull elements. The parameters of the
four-bar systems are given in Table
2.
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For the calculation of the forces the bill tips were considered to be in their rest position, except for depression forces of the upper bill, which were calculated for the rest position and for 10° elevation. The following forces were calculated: (1) the muscle force available for intentionally elevating the upper bill (Elev. UB), (2) the muscle force available for counteracting external forces that might unintentionally elevate the upper bill (Depr. UB), and the maximal jaw closing force (Max. close). All forces are summarised in Table 3.
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The forces available to elevate the upper bill are similar among species. The muscle forces and shape of the four-bar system are also similar, which indicates that all morphologies are equally able to transfer the force of their opener muscle onto the bill tip. Comparison of the opening force with Fig. 10 shows that this muscle force is sufficient for elevation of the upper bill within the physiological range for all species (ignoring the forcelength relationships of the muscle and the small change in direction of the muscles as the quadrate swings forward).
The calculated depression forces of the upper bill differ among the three species. Both the ostrich and the rhea are capable of producing larger depression forces than the emu. There are no large differences in orientation of the muscles between the species and the low value for the emu is largely explained by its relatively small muscle forces and the acute angle of the quadrate. It must, however, be noted that the emu, which has a relatively low muscle force to counteract external forces, has the highest intrinsic elastic force in the bones to counteract bending (Fig. 10). The comparison of the depression forces generated in rest and elevated positions show that these forces decrease when the bill is elevated. This decrease is partly compensated by the increase in elastic force from the kinetic hinge.
Biting forces are relatively low. The ostrich produces the largest biting force, which is explained by its relatively short bill, and therefore relatively small moment arm for the bill tip. The relatively low biting forces of the emu are explained by the relatively small mass of the jaw muscles.
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Discussion |
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Bending zones are clearly recognisable in both the dorsal and ventral bars
of the upper bill in Calidris species, which are neognathous
rhynchokinetic birds. The position of these bending zones coincides with the
bending point determined from behavioural analyses
(Gerritsen, 1988). The bending
zones in the palaeognathous species are not clear, although the bars are
relatively more slender than in Calidris. All the palaeognathous
species analysed in this study have the thinnest zones in the dorsal bar near
the caudal or rostral part of the dorsal bar, outside the effective bending
limits of the upper bill. This indicates that no clear bending zone is present
in the dorsal bar of the Palaeognathae. Although the thickness curve of the
ostrich shows some resemblance to that of the Calidris species, note
that the slender part is directly behind the rostrum maxillae. This rostrum is
very thick and semicircular, which makes this region very rigid and difficult
to bend. The ventral bar of the Palaeognathae shows a slight decrease in
relative thickness, but this is far less pronounced than in the
Calidris species. Also the position of the thinnest parts of the
ventral bars is situated very caudal in the bill, beyond the most rostral part
of the very large rostrum parasphenoidale. This bony element protrudes very
far rostrally and becomes a part of the upper bill. It is very rigid and
opposes bending in the caudal part of the upper bill. As rostral bending in
the upper bill is opposed by the rigid rostrum maxillare, and caudal by the
rostrum parashenoidal, the area suitable for bending is very small (Figs
7,
8,
9). This indicates that bending
in the caudal part of the bill will be very limited, and confirms that bending
is absent in the caudal part of the bill, as shown in behavioural analyses
(Gussekloo and Bout,
2005
).
Another feature of a rhynchokinetic skull is the ability to overcome the
elastic forces in the upper bill as a result of bending by muscle force. As
shown here, the forces opposing bending in the upper bill of the Palaeognathae
are not very high, which means that bending in the upper bill can easily occur
as a result of internal or external forces. The calculated muscle forces for
upper bill elevation in palaeognaths are large enough to overcome the
intrinsic elastic forces opposing elevation, indicating that self-induced
elevation of the upper bill (induced kinesis) is possible. However, the
elastic forces in the upper bill of the palaeognathous species increase
continuously with elevation of the upper bill. This linear increase in
resistance seems significantly different from the force reported for
(prokinetic) finches (Nuijens and Bout,
1998), where the resistance to upper bill elevation is close to
zero over most of the physiological elevation trajectory but then starts to
increase exponentially. Since upper bill resistance is very low in prokinetic
birds it can be hypothesized that the bill of the palaeognathous species is
not optimised for self-induced movement.
On the basis of the findings in this paper, we conclude that the total
configuration of the bony elements is not adapted to large bending in the
upper bill, even though bending does occur in the upper bill of palaeognathous
species (Gussekloo and Bout,
2005). The relatively high resistance of the upper bill compared
to prokinetic birds, and the lack of clear bending zones, indicate that the
morphology of the Palaeognathae is not `designed' for elevation of the upper
bill. This implies that the function of cranial kinesis in palaeognathous
birds is not the same as in neognathous rhynchokinetic birds, such as the
Charadriiformes. The bending in the upper bill of palaeognathous species is
more likely to be an unwanted effect of the slenderness of the lateral and
dorsal bars.
Our findings on jaw closing force also contradict part of the hypothesis of
Zweers et al. (1997). They
assume that the presence of a moveable palate, in combination with a large
pterygoid muscle, results in higher biting forces. Although there are very few
data on biting force in birds it is clear that the biting force calculated
here for palaeognaths is very low. Even finches with much lower muscle masses
are able to produce forces similar to those found in the ostrich
(Simms, 1955
; van der Meij and
Bout, 2000
,
2004
).
In our analysis we found that the musculus pterygoideus has very little
effect on the biting force. Remarkably, this situation is also seen in
lizards, where a large pterygoid muscle is also present, but without any large
contribution to biting force (Herrel et
al., 1999). The main role of the pterygoid muscle in birds that
lack a blocking processus basipterygoideus (e.g. finches) is to balance the
retraction component of the adductor muscle, which tends to retract the lower
bill and quadrate. In these birds the component of the pterygoid muscles that
contributes to jaw closing is relatively small.
In the Palaeognathae the retraction component of the lower jaw closers can be balanced by the reaction force on the processus basipterygoideus. This process blocks caudal movement of the pterygoid and blocks depression of the upper bill beyond the resting position.
Additionally, in the palaeognathous morphology part of the pterygoid muscle does not attach to the mandibula but has its origin on the processus basipterygoideus. The function of this part of the muscle is therefore retraction of the PPC only. The combination of these two features can be used to overcome external forces that might act in such a way that they would elevate the upper bill. Such forces are present during grazing in the Palaeognathae. During grazing leaves are pulled forcefully from plants or the ground by a fast ventrocaudally directed, jerky movement of the head and neck. Such a movement generates external forces varying over time that, due to the low intrinsic elastic forces of the bones, might induce unwanted elevation of the upper bill. The processus basipterygoideus acts as a stabilizer for this varying load. The two main muscle complexes, the lower jaw adductors and the pterygoid muscles, can be continuously maximally active and the caudally orientated component of these muscles pulls the pterygoid tight against the processus basipterygoideus. This will stabilise the upper bill and the muscles do not have to adjust their activity to balance the variable external force on the upper bill. Only if the external force exceeds the intrinsic elastic force of the bones and the force produced by the pterygoid and adductor muscles will it lift the upper bill, and therefore the PPC complex, from the processus basipterygoideus. Note that the palaeognathous species with the stiffest bony configuration also has the weakest muscles and vice versa, which seems to indicate a trade-off between rigidity of the bills and jaw muscle force; in other words, a rigid configuration needs less muscle power to stabilise the upper bill, while weak configurations need muscles to stabilise the bill.
It has generally been accepted that the morphology of the palaeognathous
PPC is related to rhynchokinesis (Bock,
1963; Hofer, 1954
;
Simonetta, 1960
). Our
findings, however, do not support this hypothesis. From the force analysis we
conclude that the processus basipterygoideus in combination with the jaw
muscles acts as a stabilizing mechanism that helps to resist varying external
forces that might otherwise elevate the upper bill. The idea that the large
pterygoid muscle in combination with the processus basipterygoideus acts as a
stabilising mechanism is also confirmed by the overall configuration of the
skull. A large rostrum parasphenoidale is found in combination with an almost
completely ossified palate, with very broad bones. In neognathous birds the
bones tend to be more slender, especially when no muscles are attached to it.
The overall configuration seems to reflect a demand for stabilising of the
upper bill and enlarging the amount of bone in the palatal region.
Plausible evolutionary scenarios to explain the morphology of the skull of
the Palaeognathae are difficult to postulate. The ancestor of the
Palaeognathae was probably a small, flying, species with a kinetic skull and a
morphology similar to that of the present day Tinamiformes. A reduction of the
lateral aspect of the skull, as observed in the Palaeognathae, can already be
observed earlier in evolution with the increased fenestration of the
vertebrate skull (Zweers et al.,
1997). The ability to fly may have contributed to a further
reduction of head weight, e.g. the bony elements of the skull. Although the
Palaeognathae became secondary flightless it would still be advantageous to
keep the total weight of the skull on top of the long neck as low as possible,
especially considering the large increase in size of these species. To reduce
weight a further reduction in bony elements may have occurred, mainly in the
lateral cranial bars (lateral bar of the upper bill, pre- and postorbital
bones). One possible selective force favouring a kinetic upper beak may be
that simultaneous movement of the upper and lower jaw increases the speed of
opening and closing. This would be advantageous for species feeding on active
prey (see Herrel et al.,
2000
). On the other hand, for tearing of plant material an
akinetic upper jaw seems more suited. Forces acting against external loading
would not be generated by muscles but by the bony material of the skull. This
seems in agreement with the observation that cranial kinesis is strongly
reduced in lepidosaurs that use their tongue to catch prey or feed on plant
material (Arnold, 1998
). When
Palaeognathae shifted their diet to a largely herbivorous one, the skull
needed reinforcement for the upper bill to resist unwanted bending due to
external forces. This was achieved by reinforcement of elements in the ventral
aspect of the skull (PPC), and the loss of bending zones. Both skull mass and
the fact that part of their diet is still made up of insects and small
vertebrates, might contribute to the preservation of cranial kinesis, but
without detailed knowledge of the feeding mechanism and external forces acting
on the skull it not clear why Palaeognaths do not reinforce the ventral and
dorsal bar of the upper beak until it becomes akinetic.
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Acknowledgments |
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