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First published online November 2, 2007
Journal of Experimental Biology 210, 3955-3961 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008953
Functional significance of the uncinate processes in birds
1 Faculty of Life Sciences, University of Manchester, Jackson's Mill, PO Box
88, Sackville Street, Manchester M60 1QD, UK
2 Institute for Zoology, Bonn University, Germany
* Author for correspondence (e-mail: jonathan.codd{at}manchester.ac.uk)
Accepted 29 August 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: biomechanics, breathing mechanics, morphology, uncinate
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) and do not
ventilate their lungs by expanding the lung itself, but through the
bellows-like movement of air through the air sacs
(Brackenbury, 1972;
Brackenbury, 1973). Uncinate
processes are bony projections that extend from the vertebral ribs of most
extant birds (Fig. 1). In 1935,
Zimmer postulated that the uncinate processes played some role during
inspiration (Zimmer, 1935).
Contemporary hypotheses have linked these processes with stiffening or
strengthening the rib cage (Kardong,
1988; Walker and Liem,
1994), providing attachment sites for muscles stabilizing the
shoulder (Hildebrand, 1982),
or serving as an adaptation for flight
(Welty and Baptista, 1988).
Existing hypotheses on uncinate function appear to have been based on the
general morphology of these structures rather than experimental analyses.
However, recent electromyographic studies in the giant Canada goose confirmed
Zimmer's hypothesis by demonstrating that these processes are integral
component of the ventilatory mechanics of birds being involved in both
inspiration and expiration (Codd et al.,
2005). The processes are associated with fleshy parts of the Mm.
intercostales externi, the Mm. appendicocostales that originates from the
proximal edge of the uncinate and inserts onto the following vertebral rib
(Shufeldt, 1890). The Mm.
appendicocostales is active during inspiration in the giant Canada goose,
suggesting the processes facilitate the craniad movement of the ribs, which
would in turn move the sternum ventrally
(Codd et al., 2005). The base
of the uncinate processes serves as a brace for the insertions of the
`finger-like' projections of the M. externus obliquus abdominus that pull the
sternum dorsally during expiration (Codd et
al., 2005). Given that the processes provide attachment sites for
these important respiratory muscles, any change in uncinate morphology may
have a significant effect on ventilation. Here we develop a mathematical
mechanical model to examine the mechanics of ventilation in birds. This model
will then be used to determine the mechanical advantage of the uncinate
process system for movements of the ribs and therefore sternum during
respiration.
|
;
Patak and Baldwin, 1993;
Dyke and Rayner, 2001;
Rayner and Couldrick, 2003;
Zeffer and Norberg, 2003).
Furthermore, variations in uncinate morphology have previously been
anecdotally linked to differences in locomotor mode, and long uncinate
processes noted in diving species (Welty,
1988; Duncker,
1971); however, there has been no further examination or testing
of these observations. Here we use morphometric analysis to test the
hypothesis that the length of the uncinate processes is predominantly
correlated with the locomotor mode of birds. We will then use our mechanical
model to examine the functional significance of these differences in uncinate
length. In light of our mechanical model, a demonstrable link between the
locomotor mode and the length of the uncinate processes will enable us to gain
a better understanding of breathing mechanics in Aves.
The geometrical model of uncinate function
At a first approximation, the ribcage of a bird can be considered to be
composed of two sets of dorsal and ventral ribs, which are held the same
distance apart at the backbone and sternum, and at the same angle. Hence the
dorsal and ventral ribs can be regarded as mirror images, which are separated
where they join by the same distance as at the backbone and sternum. Therefore
two adjacent dorsal ribs can be modeled as the opposite sides of a
parallelogram (Fig. 2), running
at an angle 
to the backbone and separated from each other by a
distance D. Moving such a mechanism is clearly very different from
rotating a single bone about a single joint. Any muscle can only alter the
angle of the ribs to the backbone, and its mechanical advantage is
best described by determining how much it changes in length for a given change
in the rib angle; the bigger the length change, the more powerful its action
and the greater its mechanical advantage.
|
 | (1) |
 | (2) |
), which demonstrated that the Mm. intercostalis externus had
no activity related to either inspiration or expiration but was active during
contralateral limb support, suggesting it plays a role acting as a brace to
stabilise the thorax during locomotion
(Codd et al., 2005).
For the appendicocostales muscle, however, for which P is
positive, the length of the muscle will vary with the angle of the ribs
according to the modified version of Eqn
1.
 | (3) |
increases, so the appendicostales muscle
will act to swing the ribs forward. Two examples of how the muscle's length
will vary with are shown in Fig.
3A for P=0.5D and P=D. It can
be seen that the length changes more rapidly with for larger values of
P (the higher the angle of the muscle to the backbone) and at higher
values of (the higher the angle of the ribs to the backbone).
Therefore the mechanical advantage of the muscle will alter with both
P and . Mechanical advantage (MA) is defined as the relative
change in muscle length per unit change in angle and is given by the formula:
 | (4) |
, and is higher for larger
values of P.
|
 | (5) |
rises the reduction
in the distance x parallel to the ribs
(Dcos+P) is unaffected, the increase in the distance
perpendicular y to the ribs (Dsin–Q)
is reduced. Indeed if Q is sufficiently large that the uncinate
process extends behind the posterior rib, swinging the ribs forward will
actually reduce the perpendicular distance. The effect of uncinate processes
of length Q=0.5D and Q=D on the length of
the appendicocostales at different angles are shown in
Fig. 3A, and the mechanical
advantage at different angles is shown in
Fig. 3B. It can be seen that
the change in muscle length and the mechanical advantage of the muscle is
greatly increased by the uncinate process, giving a good mechanical advantage
even at low values of . The uncinate acts as a mechanical lever, being
most effective when it is longer and, surprisingly, when P is
smaller.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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of the ribs were measured in four randomly chosen representative bird species:
the diving razorbill Alca torda L.; the non-specialist locomotors
kestrel Falco tinnunculus L. and barnacle goose Branta
leucopsis Bechstein 1803; and the walking red-legged partridge
Alectoris rufa L. All lengths were measured on the left hand side of the skeleton using a digital caliper (16EX 150 mm, Product No: 4102400, Mayr GmbH, Berlin, Germany), while the angle was measured using an image analysis system of digital images. Using our mechanical model (Eqn 4), we then calculated the mechanical advantage for each appendicocostales muscle, with and without the uncinate processes.
Skeletal morphology
Data were collected from the skeletons of 100 birds representing examples
from all major taxa and orders (see Appendix in supplementary material). To
establish if within-species variation in uncinate process length on different
ribs was significantly different, the lengths of the processes from ten
skeletons of adult barnacle geese Branta leucopsis were examined.
Birds were then grouped according to specialization to a primary mode of
locomotion. (1) Walking, including birds that are either flightless (e.g.
cassowary) or incapable of sustained flight (e.g. capercallie); (2) diving,
including all birds that actively forage under water by either plunge (e.g.
kingfisher) or sustained, deep diving (penguin); and (3) non-specialists,
including all other birds flying or swimming that are not facultative diving
or walking birds. We collected measurements of the length of the vertebral and
sternal ribs, and the length and width of the uncinate processes. Sternal
morphology was also examined by measuring the total length and depth of the
sternum (height of keel). Correcting for body size is problematic in birds as
many species have disproportionably long necks, meaning the traditional
snout–vent measurements to scale for size are not feasible. Therefore
all data collected were corrected for variations in body size by dividing
total length by the length of the vertebral column spanning the thoracic ribs.
All data were collected from the left hand side of the skeleton using a Mayr
digital caliper (16EX 150 mm, Product No: 4102400, Mayr GmbH).
Statistical analysis
Relationships between the groups were determined using canonical variate
analysis (CVA), which maximises the variation between groups relative to the
variation within groups (Campbell and
Atchley, 1981). Values used in the CVA were: uncinate length and
width at base, midpoint and tip; sternal width, length and depth; vertebral
and sternal rib length. A one-way ANOVA with a Tukey post-hoc test
was used to establish if mean uncinate length varies according to mode of
locomotion. Within-species uncinate comparison and the ratio of sternal length
to depth were analysed using a repeated-measures ANOVA with Bonferroni
comparisons. All analyses were completed using the statistical package SPSS
(SPSS v.13.0; SPSS Ltd, Chicago, IL, USA).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Rib cage morphology
Rib number does not always correlate with locomotor mode, although walking
species generally tend to have the fewest ribs and the diving species the
most. For birds used in this study, 8 had 6 ribs, 43 had 7 ribs, 25 had 8
ribs, 22 had 9 ribs and only 2 had 10 ribs (see Appendix in supplementary
material). Our correction for body size will tend to make comparisons less
different rather than more. The general morphology of the rib cage was similar
in all birds examined, as indicated by a within-species comparison of relative
uncinate process length (mean ± s.e.m.) for 10 barnacle geese
Branta leucopsis. Aside from the first rib, sternal ribs connect the
vertebral ribs to the sternum and these become increasingly thinner and longer
as one moves down the vertebral column. Using one-way ANOVA and Tukey
post-hoc tests the mean length (± s.e.m.) of the uncinate
processes are significantly shorter on the first (0.16±0.02) and last
(0.14±0.02) ribs on which they occur. Therefore data from these
processes were not used in the canonical analysis. The processes on the
remaining ribs are not significantly different in length (rib 2:
0.22±0.03; rib 3: 0.23±0.02; rib 4: 0.22±0.02; rib 5:
0.21±0.03). Therefore the mean length of processes 2–5 was used
in all subsequent analyses.
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Uncinate morphology
The relative length of the uncinate processes was found to be more similar
in birds with the same locomotor mode. They were shortest in the walking
(0.11±0.02, N=10, P<0.01), of intermediate length
in non-specialist (0.17±0.01, N=66, P<0.01) and
the longest in diving species (0.23±0.01, N=24,
P<0.01). The processes of the walking birds typically reach about
halfway across to the following rib. In non-specialists the processes have a
characteristic L-shaped morphology and reach across to the following rib. In
diving species the uncinate processes are long, thin and taper towards the end
(Fig. 1C), and may overlap the
following rib. There is no significant difference between relative uncinate
length in the deep (0.21±0.01, N=8) and shallow divers
(0.19±0.02, N=16, P=0.32, two-sample
t-test).
Sternal morphology
The relative ratio of sternal length to depth of walking birds was
significantly lower (1.12±0.44, N=10, P<0.001)
than that of non-specialist (2.16±0.07, N=66,
P<0.01) and diving species (2.75±0.20, N=24,
P<0.01).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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These results can help shed light on the two main findings of the
morphometric study: first that the anterior and posterior uncinates are
shorter than the intermediate ones; and second that the uncinates and sternum
of diving birds were relatively longer than those of walking birds, with
non-specialist birds having uncinates and sternum of intermediate length. The
sternum in birds is the site of attachment for the large flight muscle, the
pectoralis and supracoracoideus (Duncker,
1971). The pectoralis can account for up to 35% of the body mass
of some birds (Dial et al.,
1988). This large muscle mass, together with the abdominal
viscera, must be moved up and down during breathing
(Brainerd, 1999). The
importance of movements of the sternum is highlighted by the entrainment of
wing beat with sternal movements (Jenkins et al., 1998) and the fact that
birds can suffocate if movements of the sternum are restricted (Ludders et
al., 2001). The uncinate processes also act as a brace for the insertion of
the M. obliquus externus, which pulls the sternum dorsally to effect
expiration (Codd et al., 2005),
meaning there is a functional link between sternal and uncinate morphology and
the breathing mechanics in birds. The sternum of walking birds is reduced and
this group has the shortest length processes, while the elongated sternum of
diving birds correlates with the longest length processes. Differences in
uncinate morphology may translate into anatomical differences in the
associated musculature such as the Mm. appendicocostales and M. obliquus
externus, meaning that different patterns of muscle activity facilitate
breathing; this, however, remains to be determined.
The Mm. appendicocostales attaches to the proximal edge of the process,
meaning that the total length of the process is the most significant
characteristic in uncinate morphology. The width of the process along its
length may contribute to the overall strength. However, the process is rigidly
fixed from above to the rib it extends from by a strong triangular aponeurotic
membrane that is attached from the anterior edge of the process along its
entire length (Shufeldt,
1890). This ligament provides a strong anchorage for the lever
action on the ribs and may negate any thickening of the process itself. Aside
from the walking birds, the uncinate processes are also typically thin and
taper towards the tip of the process. Alterations in uncinate length may also
have implications for the area available for muscle insertion, given the role
of the processes during expiration, as thickening of the base would increase
the area for attachment for the insertion of the M. obliquus externus
(Codd et al., 2005). In all
birds examined the anterior and posterior uncinates are siginficantly shorter
than the remaining processes. Aside from the diving species, the mechanical
advantage for the anterior and posterior processes is also correspondingly
lower, suggesting these processes and their associated muscles probably have
little function in moving the ribcage during breathing.
Determination of locomotor modes
The locomotor modes used in the morphometric study are broadly defined into
walking, diving and non-specialist birds. Although within each group there
remain potentially significant differences between the birds, i.e. foot and
wing propelled divers, these modes can be considered to be representative as
there are broad mechanical differences between specialization for running
versus diving and/or non-specialists (all other birds). Swimming
birds were not categorized as a separate grouping as there are no birds that
swim but do not fly. The results of the CVA analysis indicate that there are
species that overlap or are near the border of the locomotor groups. These
species represent birds that have intermediate morphology; for example, the
fulmar (Fig. 5
), which
is classed as a diving species, is a strong flyer, which may explain why it
borders the non-specialist group. The green woodpecker
(Fig. 5ß), which clusters
close to the walking species, can be considered an atypical bird as it has
pronounced broadening of the vertebral ribs as an adaptation to head banging
(Kirby, 1980). Swallows
(Fig. 5µ) have highly
streamlined bodies, which may explain why they cluster close to the diving
species.
Contrast in uncinate morphology between diving and walking species
Longer processes have previously been assumed to play a role in preventing
collapse of the rib cage by counteracting the increased pressure with
increased depth during dives (Welty,
1988). However, aside from the penguins (Aptendytes
patagonicus, Spheniscus demersus and S. humbolti) and auks
(Pinguinis impennis, Alca torda and Alle alle), the vast
majority of diving birds investigated in this study do not dive to depths
likely to encounter large increases in pressure. Species from diverse groups
such as the kingfisher (Alcedo atthis), the white throated dipper
(Cinclus cinclus), the gulls (Larus argentatus and L.
canus), the ducks (Clangula hyemalis and Mergus
merganser) and the terns (Sterna paradisaea and S.
hirundo) have nominal diving depths of less than 10 m; i.e. approximately
1 atmosphere of pressure (Jones and
Furilla, 1987). Despite this, there is no significant difference
between uncinate length in the deep and shallow divers; all diving birds have
significantly longer uncinates than the non-specialist and walking birds (see
Appendix in supplementary material). Any muscle pulling on the uncinate
processes will facilitate movement of the associated rib rather than prevent
it. Furthermore, given that the uncinate processes are not found on every rib,
it seems unlikely that they are essential in stiffening the body cavity
against increased pressure. The caudally located thin and long ribs, i.e.
those that would need the most stiffening as pressure increased on the rib
cage, lack uncinates (Fig. 1C).
Diving birds have a streamlined body form, long ribs and sternum, to reduce
resistance on entry to the water. In diving birds the greater relative length
of the uncinate processes is probably related to the greater length of the
sternum and the lower angle of the ribs to the backbone and sternum
(Fig. 1C). As indicated by our
model, without an uncinate process the mechanical advantage of the Mm.
appendicocostales in lowering the sternum is low, while the force needed to
lower the sternum against the large pectoralis muscle in these species would
be extremely high. Interestingly, in the razorbill the effectiveness of the
uncinate process at increasing the mechanical advantage was actually rather
low. This is probably due to the large angle between the ribs and the
vertebral column in this species, which may make the uncinate less important,
but it contrasts strongly with the low angle seen in its relative the
guillemot (J.R.C., unpublished observations). During surfacing both penguins
(Wilson et al., 2003) and
tufted ducks (Parkes et al.,
2002) maximise gas exchange by increasing breathing frequency. The
increased mechanical advantage of longer uncinates may be especially important
upon resurfacing when inspiration occurs against the pressure of water against
the body. In walking birds, in contrast, the sternum is relatively small
(Fig. 1A) and the ribs are at a
large angle to the backbone and sternum
(Fig. 2A). Even without an
uncinate process the appendicocostales muscle could have a reasonable
mechanical advantage, and little force needs to be exerted against the tiny
pectoralis muscle. In any case the dorsal and ventral ribs tend towards being
parallel, meaning that rotating the dorsal rib forward would have little
effect in increasing the volume of the chest cavity.
Conclusion
The morphology of the rib cage and the length of the uncinate processes
varies with locomotor mode. The reduction in uncinate length found in the
walking species suggests that they may play a reduced role during breathing in
these species, meaning muscles such as the Mm. intercostalis externi may play
a significant role during inspiration in walking birds; this, however, remains
to be determined. The elongation of the ribs, rib cage and sternum associated
with streamlining in diving species suggests that differences may also exist
in their breathing mechanics. Given the increased length of the processes in
diving birds, the insertion of the Mm. appendicocostales towards the end of
the tip of the processes may further improve the mechanical advantage for
moving the elongated ribs during breathing. Future work may improve our
understanding of anatomical differences in musculature associated with
variations in uncinate morphology. Alternative functions of the uncinate
processes remain to be determined; for example, the role of the uncinate
processes in stabilizing the scapula during retraction of the wing has not
been examined here. Additionally the `finger-like' projections of the M.
obliquus externus abdominus insert onto the base of the processes, and in the
opposite manner the M. serratus superficialis originates at the top of the
processes and inserts on the ventral margin of the scapula
(Vanden Berge and Zweers,
1993), suggesting that they may act antagonistically. Variations
in uncinate morphology seem likely to relate to differences in the muscles
involved in breathing or in the pattern of muscle activity. Respiration in
Aves is complex, with a great many axial muscles reported to be involved
(Fedde, 1987). This research
suggests that there may be fundamental differences in the breathing mechanics
of different birds, driven in part by the morphological differences of the rib
cage and sternum associated with skeletal adaptations to locomotion.
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Acknowledgments |
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Footnotes |
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