Scaling of jaw muscle size and maximal bite force in finches
Department of Evolutionary Morphology, Institute of Biology Leiden, PO Box 9516, 2300 RA Leiden, The Netherlands
* Author for correspondence (e-mail: meij{at}rulsfb.leidenuniv.nl)
Accepted 18 May 2004
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Summary |
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Key words: bite force, muscle, allometry, finch, fringillid, estrildid, seed, husking
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Introduction |
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Although body size may play an important role in establishing differences
in husking performance and therefore in occupying different trophic niches
(Björklund and Merilä,
1993), family-specific differences in seed handling efficiency
have been reported. Cardueline finches are much more efficient at handling
large seeds than are emberizine sparrows, which may be related to a difference
in jaw muscle mass (Benkman and Pulliam,
1988
). The jaw muscles of oscines are described in several studies
(Fiedler, 1951
;
Beecher, 1953
;
Classen, 1989
;
Nuijens and Zweers, 1997
).
Nuijens and Zweers (1997
)
suggested that there are differences in relative jaw muscle weight between
estrildids and fringillids, which belong to two separate families. These two
groups of finches differ in their ability to crack seeds efficiently:
fringillids crack closed-shelled seeds faster than estrildids (R. G. Bout, R.
Verbeek and F. W. Nuijens, manuscript submitted). The diet of fringillids
consists of a wide range of seeds, including many closed-shelled
dicotyledonous species (e.g. Compositae; Newton,
1967
,
1972
). Many estrildids feed
mainly on small, soft (monocotyledonous) grass seeds
(Read, 1994
;
Zann, 1996
;
Dostine et al., 2001
). Some
estrildid species (e.g. Erythrura, Spermophaga poliogenys), however,
feed on a wide range of dicotyledonous seeds
(Clement et al., 1993
). This
difference in diet suggests that fringillids are able to take seeds of a wider
range of hardness and are able to produce higher bite forces than estrildids.
One of the few attempts to measure bite force in birds directly was made by
Lederer (1975
). Recently, A.
Herrel (personal communication) measured maximal bite forces in Galapagos
finches.
The present study will try to establish the relationship between body size, jaw muscle mass and maximal bite force in two groups of finches: the estrildids and the fringillids. We will investigate whether there are significant differences in jaw muscle size and bite force between estrildids and fringillids of the same body size. Furthermore, the scaling of muscle fibre length relative to body mass is studied to investigate how muscle mass is related to muscle force (physiological cross section).
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Materials and methods |
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The nomenclature of the muscles follows Vanden Berge and Zweers
(1993). Five groups of muscles
were distinguished: (1) the openers of the lower jaw, musculus depressor
mandibulae; (2) the closers of the lower jaw, musculus adductor mandibulae
externus and musculus pseudotemporalis superficialis; (3) the openers of the
upper jaw, musculus protractor pterygoidei et quadrati; (4) the closers of the
upper and lower jaw, musculus pseudotemporalis profundus and musculus adductor
mandibulae ossis quadrati and (5) the closers of the upper and lower jaw,
musculus pterygoideus, including the musculus retractor palatini. After
dissection of the muscle groups, the mass of each group was measured with a
digital balance (H51; Sartorius).
To allow a first comparison between the data for the fringillids and
estrildids and the scaling of jaw muscles mass within the class Aves as a
whole, we also measured the jaw muscle mass of 12 bird species with body mass
ranging from 12 to 12 000 g (Table
2). Furthermore, we used data from three studies that reported jaw
muscle mass and body mass. Scaling exponents were calculated for the data from
seven Serinus species (Classen,
1989), four cormorant species
(Burger, 1978
) and 14
anseriform species (Goodman and Fisher,
1962
).
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An expected value for the scaling of jaw muscle mass with body mass may be
derived from the scaling of other head structures. Therefore, we used data of
the head mass of eight anseriforms (Van
der Leeuw, 2002) and compared the scaling of jaw muscle mass to
eye (Brooke et al., 1999
) and
brain mass in birds (Schmidt-Nielsen,
1984
).
Muscle fibre length
Muscle force is expected to scale with cross-sectional area of muscles. To
evaluate the relationship between muscle mass and muscle force, the scaling of
muscle fibre length with body size should be known. To determine scaling of
muscle fibre length, the musculus adductor mandibulae externus from 10
Fringillidae species was preserved in alcohol. This muscle complex was chosen
because it is the main jaw closer. Although there are differences in fibre
length between the different jaw muscle groups (M. A. A. Van der Meij,
unpublished data), the scaling of adductor fibre length is believed to be
indicative for all muscle groups.
To obtain the fibre length, we used the protocol described by Herrel
(1998). The collagen between
the muscle fibres was gradually dissolved in nitric acid (31% HNO3)
for about 24 h and then the tissue was immersed in a 50% glycerol solution.
Muscle fibres were selected at random from the dissected muscle, carefully
teased from the tissue and their length measured under a Nikon microscope.
Bite force measurements
To measure the maximal bite force of the finches we used a force transducer
(9000 series; Aikoh, Osaka, Japan) mounted with two flat metal plates
(Fig. 1). Biting causes the
upper plate to pivot around a fulcrum and to exert force on the force
transducer. The birds were held by hand and trained to bite the metal plates.
Most birds only used their beak tips to bite the force transducer and refused
to bite at more caudal positions within the beak. The rounded ridge of the
plates limited the biting area to a specific part of the beak and prevented
pressure from the rest of the bill. The force transducer was set to register
the peak force, which was read from the display. Before the experiments, the
force transducer was calibrated by applying known forces to the plates. The
accuracy of the force transducer is 0.1 N, while the measuring range of the
force transducer was between 0 and 50 N. Bite force measurements were
performed several times in a row on each occasion and on at least five
different days to determine the maximum bite force at the tip of the bill. The
maximal bite force for a bird is the highest value measured, but in all cases
at least two other bite forces were recorded that differ less than 0.2 N of
the maximal value.
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Data analysis
The data were log transformed to normalise the variables. As the body mass
of the fringillids in our sample is, on average, 1.8 times larger than the
body mass of the estrildids, a comparison of bite force between the two groups
should involve body mass as a covariant.
Allometric equations are of the form Y = a Xb
or logY = loga + b logX, in which
Y is the dependent variable, a is the proportionality
coefficient (the intercept), b is the exponent (slope of the
regression line) and X is the independent variable. A difference in
jaw muscle mass and/or biting force between fringillids and estrildids may
result from a difference in intercept or a difference in slope. An analysis of
covariance (ANCOVA) was used to test for the equality (homogeneity) of slopes
for the two groups. A linear model containing the main effects as well as the
interaction term is fitted through the data. The interaction term provides the
test for the equality of slopes (Quinn and
Keough, 2002). Statistical tests were performed in SPSS 10.0 (SPSS
Inc., Chicago, IL, USA).
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Results |
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Jaw muscle mass
An analysis of covariance shows that for jaw muscle mass versus
body mass the interaction term (family x body mass) is not significant
(P=0.826). The common slope for the two groups of finches is 1.29
(95% CL, 1.091.50) and demonstrates a positively allometric increase of
jaw muscle mass with body mass in fringillids and estrildids. The intercepts
for estrildids and fringillids are significantly different
(P<0.001; Fig. 2;
Table 3). Total jaw muscle mass
is higher in fringillids than in estrildids.
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Muscle groups
The jaw muscles can be divided into five functional groups and their
proportions as percentage of total jaw muscle mass are shown in
Table 4. Tested for each muscle
group separately, there was no difference in the increase of muscle mass with
body mass between the two families. All the interaction terms were not
significant (all P>0.28), and the slopes for the mass of each
muscle group versus body mass are shown in
Table 4. The 95% confidence
levels of the slopes for each muscle group overlap and all include the slope
for total jaw muscle mass (1.29). This suggests that a common slope may
describe the scaling of all muscle groups (openers and closers) with body
mass. There is no significant interaction between the mass of the different
muscle groups, body mass and the two families (P=0.47), and the
common slope for the five muscle groups x two families was estimated to
be 1.24 (P<0.001; Fig.
3).
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Total jaw muscle mass is higher in fringillids than in estrildids. To check whether this difference in total jaw muscle mass is the result of a single muscle group or the result of a general increase in mass of all muscle groups we tested the difference in intercepts between the two families for each muscle complex (Fig. 3). The adductor complex (P<0.001), the quadrate adductors (P=0.005) and the pterygoid complex (P=0.018) are significantly heavier in the fringillids than in the estrildids relative to body mass. The mass of the protractor complex (P=0.248) does not differ between the two families, while the depressor complex (P=0.046) is minimally significant.
Bite force
As jaw muscle mass increases relative to body mass, the maximal bite force
at the tip of the bill is also expected to increase with body mass (see
Fig. 4). The analysis shows
that the slopes for the estrildids and fringillids do not differ significantly
(interaction term, P=0.254). Bite force increases positively
allometric with body mass (slope, 1.44; 95% CL, 1.181.69). As for jaw
muscle mass, the intercepts of the regression lines for bite force differ
significantly (P=0.012) between estrildids and fringillids: the bite
force in fringillids is 1.4 times higher than in estrildids of the same body
size.
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The slope for bite force versus jaw muscle mass is 1.05 (95% CL, 0.871.23; Table 3). The relationship between bite force and jaw muscle mass is similar between fringillids and estrildids. There is no significant difference in slope (ANCOVA with interaction term P=0.070) or intercept (P=0.592) between the two groups. Note that within each group there is substantial variation in bite force among species independent of jaw muscle mass (Fig. 3). The partial correlation between bite force and jaw muscle mass controlling for body size is significant in fringillids (r=0.754, P=0.007) or close to significant in estrildids (r=0.419, P=0.08). This indicates that differences in bite force among species within a single group are also related to differences in jaw muscle mass.
Muscle fibre length
To investigate the relationship between jaw muscle mass and jaw muscle
force, the muscle fibre length of the adductor complex of the fringillids was
determined (Table 5). The fibre
length of the adductor complex scales negatively allometric with body mass
(slope, 0.26; Table 6).
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Discussion |
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Scaling of head, jaw muscle mass and body mass in birds
A comparison with other groups of birds or an expected value is necessary
to assess the scaling exponent for the relationship between jaw muscle mass
and body mass in finches (1.29; 95% CL, 1.091.50). Data on other groups
of birds are not available from the literature, but exponents were calculated
for jaw muscle data from three studies that reported muscle mass and body mass
(Table 6). The jaw muscle mass
of seven Serinus species (Classen,
1989) scales with an exponent of 1.31, and the jaw muscle mass of
four cormorant species (Burger,
1978
) scales with an exponent of 1.29 (95% CL, 0.4922.10),
but the exponent for the jaw muscle mass of 14 anseriform species
(Goodman and Fisher, 1962
) is
only 0.45 (95% CL, 0.1250.766; Table
6).
An expected value for jaw muscle mass may be derived from the scaling of
head size. Geometric scaling of jaw muscle mass with body mass would result in
a scaling exponent of 1.0. However, head size and head mass seem to scale
negatively allometric with body size in birds. In eight anseriform species,
head mass scales with an exponent of 0.70 relative to body mass
(Van der Leeuw, 2002). The two
largest organs that are contained in the cranium, the eye and the brain, also
show negatively allometric scaling with body size. In birds, eye mass
(Brooke et al., 1999
) and brain
mass (Schmidt-Nielsen, 1984
)
scale with a factor of 0.67. From these exponents for mass, one may expect an
exponent for linear dimensions of 0.67/3=0.22. This is in agreement with the
exponent we found for cranium length (0.28; 95% CL, 0.200.36;
Table 6) and muscle fibre
length (0.26; 95% CL, 0.150.38;
Table 6) in finches.
From these data on the scaling exponents of head structures, we conclude that jaw muscle mass may be expected to show negative allometry with respect to body size, when it scales proportional to other head structures. To check this expectation we measured jaw muscle mass in a small sample (N=12) of species from different bird families and with a wide range of body mass (Table 2). The scaling exponent for this group is 0.78 (95% CL, 0.5491.019), which is compatible with the idea that jaw muscles generally scale proportional to head size. These results show that jaw muscle mass scales positively allometric with body mass in granivorous finches and increases much faster with body size than in other birds.
Jaw muscle size and bite force
Jaw muscles are relatively larger in fringillids than in estrildids and
there are significant differences in the intercept for each complex between
the fringillids and estrildids. All the jaw closers the adductor
complex, the quadrate adductors and the pterygoid muscles differ
significantly between the two groups, while the opener of the upper jaw does
not differ significantly and the opener of the lower jaw is only minimally
significantly different between the fringillids and estrildids. The relatively
larger jaw muscle mass in the fringillids is mainly the result of the enlarged
jaw closing muscles and is directly related to their larger maximal bite
force.
Differences in maximal bite force may depend on differences in jaw muscle force but also on differences in the geometry of the cranial elements, the configuration of jaw muscles (lines of action) and beak length.
Muscle force scales with cross-sectional area of muscles. The length of the adductor muscle fibres scales against body mass with an exponent of 0.26, which means that cross-sectional area scales with an exponent of 1.290.26=1.03. This exponent is very similar to the exponent found for the relationship between bite force and jaw muscle mass. Similarly, a slope of 1.05x1.29=1.35 is expected for the relationship between bite force and body mass (compare with 1.44 found) This suggests that there are no large systematic changes in the orientation and position of muscles with respect to joints (changes in moment arms) that contribute to an increase in bite force with body size.
Differences in maximal bite force may depend on differences in the geometry
of the cranial elements. A high upper bill (kinetic hinge), for instance, is
often interpreted as an adaptation to large bite force because it increases
the moment of the upper jaw closing muscles
(Bowman, 1961;
Bock, 1966
). Whether there are
systematic differences in skull morphology between fringillids and estrildids
that contribute to differences in bite force will be investigated in a
separate study. However, the contribution of differences in skull morphology
may be limited. Jaw muscle mass and taxon described in this study already
account for 88.5% of the variation in bite force (adjusted R-squared
ANCOVA on log-transformed data).
Furthermore, there is no difference in the relationship between jaw muscle mass and bite force between the two groups that would indicate an effect of skull morphology on bite force independent of muscle force.
The comparison between fringillids and estrildids assumes that the beak length is the same for both groups. When beak length of the birds for which bite force is measured is analysed (ANCOVA) the beak of estrildids is 1.23 times longer than the beak of fringillids with the same body size. For the body size range of the finches in this study, this difference in relative beak length corresponds to a difference of 13 mm in the relative position at which the bite force was measured. As the bite force decreases with the distance to the jaw closer muscles, the lower bite force in estrildids compared with in fringillids may be the result of a longer beak. However, beak length itself is not a very accurate indicator of the position of the beak tip with respect to the jaw muscles. Morphometric analysis of the skull shows that the position of the whole beak (rictus, tip and kinetic hinge of the upper beak) may vary with respect to the jaw muscles. The length of the beak may also increase by a caudal displacement of the rictus and kinetic hinge, while the absolute position of the beak tip with respect to the jaw muscles remains the same. The small difference in beak length between fringillids and estrildids as such does therefore not explain the difference in biting force.
Jaw muscles and feeding behaviour
The large increase in biting force with body size in finches is clearly
related to their ability to produce large biting forces. A similar situation
may be present in cormorants. Cormorants capture fish, frogs and crustaceans,
which requires a powerful bite (Burger,
1978). The feeding behaviour of anseriforms (e.g. grazing,
suspension feeding), on the other hand, does not seem to require much force
and their jaw muscles' size scales with an exponent of only 0.45. Jaw muscle
mass increases much less with body size or head size (see above) than in the
finches or cormorants.
In the present study, bite forces were measured at the tip of the beak. Seeds with hardness well within the range of the maximal bite force of the bird are positioned for cracking about halfway along the length of the beak (rictus to tip). Very hard seeds are positioned more caudally. The true maximal bite force will therefore be much higher than the force measured in this study. Unfortunately, most species would only bite the force transducer with the tip of the beak.
The forces required to crack seeds that are reported in the literature are
quite high. Geospiza fortis eat Opuntia seeds that require a
force of 54 N to crack (Grant et al.,
1976). Pyrenestes ostrinus is able to feed on sedge seeds
(Scleria verrucosa) with a hardness of 151 N
(Smith, 1990
). The hawfinch
(Coccothraustes coccothraustes) is able to crack cherry stones with a
hardness of up to 310 N (Sims,
1955
). Such values are difficult to interpret without information
on contact area (applied stress) and seem to be at odds with the values for
biting force reported in the present study. The maximum bite force of the Java
sparrow (Padda oryzivora) was calculated to be 61.3 N for safflower
seeds (Van der Meij and Bout,
2000
), but the bite force measured at the tip of the beak is only
9.6 N. Although the bite force increases towards rictus level, a static bite
force model study (R.G.B., unpublished results) shows that maximal bite force
near the rictus is, at most, two times higher than at the tip of the beak.
This apparent discrepancy between seed hardness and biting force can be
resolved when the contact area between seed and bill is known. Note that the
force transducers used to determine the hardness of seeds register force
independent of contact area. In a pilot study, we measured contact areas
between seed and force transducer during cracking of the seed shell by
pressing carbon-covered seeds on paper. The maximum stresses at which
safflower seeds and hemp seeds crack were 37.8±16.1 N
mm2 and 15.5±9.3 N mm2
(N=30), respectively. To determine the contact areas between these
two seed species and the rims of the beak, the seeds were pressed on the lower
jaw of a number of freshly killed Java sparrows. The contact areas with the
beak for safflower seeds and hemp seeds were 2.39±1.07 mm2
and 1.02±0.68 mm2 (N=10), respectively. The maximal
bite force for the Java sparrow is estimated as twice the bite force at the
tip of the beak (calculations with a static force model). The contact area
between force transducer and the tip of the (upper) bill of the Java sparrow
is estimated to be 0.77 mm2, which results in a stress of
9.6/0.77=12.47 N mm2. Java sparrows are therefore able to
crack safflower seeds with a measured hardness of less than
2x12.47x2.39=59.6 N and hemp seeds with a measured hardness of
less than 2x12.47x1.02=25.43 N. These estimated values are in good
agreement with the values determined behaviourally for safflower
(Van der Meij and Bout, 2000;
61 N) and the observation that Java sparrows eat hemp readily without
rejecting many seeds. Only 4% (N=100) of the hemp seeds require
forces larger than 25.43 N to crack.
With an increase in the maximal bite force of finches, the birds may expand
the range of their diet and, thus, husking time is expected to decrease.
Husking time is directly related to seed hardness
(Van der Meij et al., in
press), and an increase in bite force may therefore be expected to
decrease husking time.
The significant difference in maximal bite force between the fringillids
and estrildids is probably also related to a difference in feeding behaviour.
The diet of carduelines consists of a wide range of seeds, containing seeds of
the family Compositae, like thistle and sunflower (Newton,
1967,
1972
). The firetail finches
(Read, 1994
), the zebrafinch
(Zann, 1996
) and the Gouldian
finch (Dostine et al., 2001
),
all estrildids, feed mainly on small soft grass seeds. This suggests that the
fringillids are able to take seeds of a wider range of hardness than are
estrildids. Why this difference between estrildids and fringillids exists is
not clear. Geographically, the two families are separated. The fringillids
occur in the Holarctic and Africa (Clement
et al., 1993
). The estrildids probably have an African origin
(Mayr, 1968
;
Clement et al., 1993
) and
inhabit the tropical east through Arabia to India and most of the Oriental
region, the Malay archipelago, New Guinea, Australia and the islands of the
South Pacific (Clement et al.,
1993
). Phylogenetic analysis shows that the two groups of finches
are separate, monophyletic clades (M. A. A. Van der Meij, M. A. G. de Bakker
and R. G. Bout, manuscript submitted). Although little is known about the diet
of finches, the information available suggests that estrildids do not explore
trophic niches with hard, closed-shelled seeds. This seems to indicate that a
(phylo)genetic constraint on jaw muscle size prevents estrildids from
acquiring bite forces that are large enough to explore niches with hard,
closed-shelled seeds.
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Acknowledgments |
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References |
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