Geospiza Bite Force
Geospiza Bite Force
Geospiza Bite Force
The relationship between shape of the skull and bite force in finches
Maria A. A. van der Meij and Ron G. Bout*
Evolutionary Morphology, Institute of Biology Leiden, Leiden University, Clusius Laboratory/EMCA, Wassenaarseweg 64, PO Box
9505, 2300 RA Leiden, The Netherlands
*Author for correspondence (e-mail: r.g.bout@biology.leidenuniv.nl)
SUMMARY
In finches husking time is non-linearly related to the ratio of seed hardness to maximal bite force. Fringillids produce larger bite
force and husk relatively hard seeds faster than estrildids of similar size. This is at least partly explained by their relatively larger
jaw muscle mass and a difference in husking technique. However, the effect of differences in skull geometry on bite force is
unclear. In this study differences in skull morphology that may contribute to the difference in bite force between fringillids and
estrildids are analyzed. The shape of the skull was described by the 3D coordinates of a set of landmarks and, after eliminating
size, the effect of differences in the shape of the skull on bite force was determined using a static force model. EMG recordings
of jaw muscles during seed cracking were used to validate assumptions about the muscle activation patterns used for the static
bite force model. The analysis shows that most of the variation in skull geometry is related to differences in size. Although the
shape of the skull is highly convergent between fringillids and estrildids, the shape of the skull differs significantly between the
two groups. A principal component analysis of the landmark coordinates shows several patterns of allometric shape changes,
one of which is expressed more strongly in estrildids than in fringillids. Three characters dominate the effect of shape changes
on bite force. Bite force increases with a more caudal position of the quadrate, a more downward inclined beak and a relatively
short jugal and palatine. A more downward inclined beak is typically found in estrildids. The height of the upper bill and a number
of other changes in skull shape have little effect on bite force. An estimate of the relative contributions of jaw muscle size and
skull geometry to the difference in bite force between fringillids and estrildids suggests that the contribution of muscle size is
much larger than the contribution of skull geometry.
Key words: bite force, feeding, finch, morphometrics, skull.
INTRODUCTION
Darwins finches and Hawaiian honeycreepers provide some of the size (Kear, 1962; Hespenheide, 1966; Willson, 1971; Schluter, 1982;
best known examples of adaptive radiation, both of which are Smith, 1987; Daz, 1990; Read, 1991; van der Meij et al., 2004).
characterised by a large diversity of beak shapes (Raikow, 1977; Although body size may play an important role in establishing
Grant, 1986). The evolutionary mechanisms underlying the differences in husking performance and therefore in occupying
divergence of feeding habits and beak morphology during adaptive different trophic niches (Bjrklund and Meril, 1993), taxon-
radiation have been studied extensively (Grant, 1986; Grant and specific differences in seed handling efficiency have been reported.
Grant, 1989). Variation in food availability and interspecific Fringillids and estrildids belong to two separate families (van der
competition result in natural selection for specific feeding habits Meij et al., 2005) and differ in their ability to crack seeds efficiently.
and beak morphologies in a number of species (Boag and Grant, Fringillids crack closed shelled seeds faster than estrildids of the
1981; Schluter and Smith, 1986; Smith, 1991; Grant and Grant, same body size and have relatively larger jaw muscles and a higher
1995) and beak size has been identified as the most variable trait maximal bite force (van der Meij and Bout, 2004; van der Meij et
in cardueline finches (Bjrklund, 1991). al., 2004). Differences in maximal bite force may depend not only
While beak size and shape may reflect the hardness and shape on differences in jaw muscle force, but also on differences in the
of the seeds taken by different species much less is known about geometry of the cranial elements (skull shape).
the variability of the traits that determine bite force directly. Bite In Galpagos finches bite force is not only related to beak size
force is influenced by body size, the geometry of the skull and jaw but also to head width (Herrel et al., 2005a; Herrel et al., 2005b).
closing muscles, and the relative size of the jaw closing muscles. While some differences in skull morphology may be the
The variation in beak shape in some groups of finches is in contrast consequence of a large bite force, e.g. by increasing the attachment
with results from studies on closely related species that show very area for jaw muscles or by increasing the resistance to reaction
little variation in beak shape and very large variation in overall size forces, other differences may be directly related to an increase in
among species (Bjrklund and Meril, 1993). The lack of divergence bite force by affecting the lever arms of muscles. A high upper bill
in beak shape in the presence of natural selection is interpreted as (kinetic hinge), for instance, is often interpreted as an adaptation to
shared adaptation to similar feeding modes (Meril and Bjrklund, large bite force because it increases the moment of the upper jaw
1999), rather than the presence of long-term developmental closing muscles (Bowman, 1961; Bock, 1966). In this study we use
constraints (Arnold, 1991). the 3D coordinates of a set of landmarks representing the positions
Most studies on the efficiency of feeding in finches concentrate of the joints between neurocranium, quadrate, pterygoid, palatine,
on husking time in relation to seed size, seed hardness and body jugal and upper and lower jaw of the skull of finches to quantify
differences in the shape of the skull between and within two groups of species were kindly made available to us by the Department of
of finches: the fringillids and estrildids. A Generalised Procrustes Experimental Zoology of Wageningen University. After removing
Analysis was used to eliminate differences in size between the skulls. most of the tissue, the skulls were cleaned with the help of enzyme-
The effect of differences in the shape of the skull on maximum enriched washing power (non-alkaline Biotex, at a temperature of
bite force was determined using a 2D static force model. EMG 37C). The lower jaw was removed from the skull to get a better
recordings of jaw muscles during seed cracking were made to check view of the ventral side of the skull.
assumptions about the muscle activation patterns used for the static
bite force model. Landmarks
To analyze the shape of the skull as well as the length of the
MATERIALS AND METHODS different skull elements we reconstructed the 3D coordinates of a
Species number of landmarks from a series of images of skulls rotated
For the morphometric analysis we used the skulls of 42 taxa: 20 along their long axis. A digital camera (Nikon Coolpix 950) was
species of the family Fringillidae and 22 species of the family set at a fixed distance of 30 cm from the skull. The digital images
Estrildidae [Table 1; taxonomical names are according to Sibley and had a resolution of 12001600 and for very small skulls the digital
Monroe (Sibley and Monroe, 1990; Sibley and Monroe, 1993)]. zoom was used (max. 2). The skulls were clamped at the top of
Most species were purchased commercially and sacrificed with an the orbital region and fixed to a rotating device in such a way that
overdose of the anaesthetic Nembutal (Sanofi Sante B.V., Maassluis, the long axis of the skull was in line with the rotation axis of the
The Netherlands). Frozen specimens (20C) from a small number device (Fig. 1). The rotating device had a wheel with a pin to select
fixed rotation intervals. The skull was then rotated along its
Table 1. Species used for morphometric analysis longitudinal axis and seven digital images were taken at 60, 30,
0, 30, 60, 90 and 120 (Fig. 2), where 0 represents a lateral
Body view of the skull and 90 a ventral view of the skull. Two metal
Family, Species Common names mass (g)
XYZ frames, one fixed to the stationary part of the rotating device
Fringillidae and one fixed to the rotation axis of the device, were used to check
Fringilla montifringilla Brambling 17.1 for unintended translations or rotation of the skull with respect to
Fringilla coelebs Chaffinch 19.9
the camera. For each skull a selected set of natural landmarks (e.g.
Carduelis carduelis European goldfinch 16.8
Carduelis cucullata Red siskin 10.8 joints, the tip of processi; see Table 2) were digitised. If necessary
Carduelis chloris Greenfinch 28.3 the position of less well-defined landmarks was marked on the
Carduelis sinica Oriental greenfinch 20.0 skull with ink (e.g. the base of processus postorbitalis) to assure
Rhodopechys obsoleta Desert finch 22.5 that the same point was measured in all images. A piece of
Rhodopechys mongolica Mongolian trumpeter finch 19.0 millimetre-marked paper was used to calculate the scaling factor
Serinus serinus Serin 11.1
for the images.
Serinus leucopygius White-rumped seedeater 9.5
Serinus atrogularis Yellow-rumped seedeater 10.4
Custom made software written in MatLab 5.3 (The Mathworks
Uragus sibericus Long-tailed rosefinch 13.0 Inc, Natick, MA, USA) was used to reconstruct the 3D coordinates
Carpodacus rubicilloides Eastern great rosefinch 36.0 of the landmarks. For each point a first estimate of its unknown
Carpodacus roseus Pallass rosefinch 21.1 third coordinate was chosen. A search matrix was created by adding
Carpodacus puniceus Red-breasted rosefinch 16.5 a random component to a series of 10 values of the first estimate
Coccothraustes coccothraustes Hawfinch 54.4 for each individual measurement. The series of photographs
Mycerobas affinis Collared grosbeak 70.0
Eophona migratoria Yellow-billed grosbeak 52.0
containing the landmark were then all rotated to the same orientation
Pyrrhula pyrrhula Eurasian bullfinch 20.8
Pyrrhula leucogenus Philippine bullfinch 22.9
Estrildidae
Padda oryzivora Java sparrow 30.4
Chloebia gouldiae Gouldian finch 15.2
Erythrura prasina Pin-tailed parrotfinch 15.4
Taeniopygia bichenovii Black-throated finch 9.7
Amandava subfava Zebra waxbill 6.8
Lonchura maja White-headed munia 13.2
Lonchura fringilloides Magpie mannikin 16.2
Lonchura caniceps Grey-banded mannikin 14.4
Lonchura stygia Black mannikin 11.1
Neochima ruficauda Star finch 12.1
Neochmia modesta Plum-headed finch 13.2
Estrilda caerulescens Lavender waxbill 8.4
Estrilda astrild Common waxbill 7.5
Pytilia melba Green-winged pytilia 13.5
Mandingoa nitidula Green-backed twinspot 13.5
Cryptospiza reichenovii Red-faced crimson-wing 14.3
Pyrenestes sanguineus Crimson seedcracker 18.0
Hypargos niveoguttatus Peters twinspot 15.7
Uraeginthus cyanocephalus Blue-capped cordon-blue 10.0
Spermophaga haematina Western bluebill 22.3
Fig. 1. Rotating device used to take photographs of a rotating skull. A, skull;
Euschistopiza dybowskii Dybowskis dusky twinspot 11.4
Amadina fasciata Cut-throat finch 18.5 b, fixed XYZ axes; c, rotating XYZ axes; d, millimeter paper; e, pin to set
the angle; f, adjustable tubes.
Fig. 2. An example of a series of images taken from a skull (6 out of 7 shown), The skull was rotated along its longitudinal axis with an interval of 30; 0
represents a lateral view of the skull and 90 a ventral view of the skull.
(0) after a correction for the projection angle. The combined gave the same results as starting with random y and z-values in the
standard deviation (s.d.) over all x, y and z measurements in the 0 0 rotation plane (x does not change under the rotation scheme used)
rotation plane was used as a cost function that was minimized with and minimizing the difference with the measured x,y values after
a steepest gradient descent method [Nelder and Mead simplex rotation of the initial coordinates towards the plane in which they
method (Bunday, 1984)] by adjusting the z-value. This effectively were measured.
The number of cycles required for the
Table 2. Landmarks of the skull algorithm to converge to accurate values
Left, right Landmark
(95% of the coordinates less than 0.002 mm
from their true value) was estimated from a
1 Most rostral point orbita data set with known values and variance.
2 Most caudal point orbita
3 Middle of frontonasal hinge
After convergence of the algorithm the final
4 Tip upper beak set of values was averaged over all
5 Most lateral connection between quadrate and skull (capitulum otic quadrati) photographs to estimate the coordinates of
6 Most medial connection between quadrate and mandible (condylus medialis quadrati) the point measured.
7 Most lateral connection between quadrate and mandible (condylus lateralis quadrati) Note that most points are not visible in
8 Most caudal connection between quadrate and mandible (condylus caudalis quadrati) all photographs. At least two photographs
9 Tip processus orbitalis quadratum
containing the landmark are required to
10 Connection jugalquadrate
11, 12c Connection quadratepterygoid estimate 3D coordinates, but the accuracy of
13 Connection palatinepterygoid the reconstructed coordinates will increase
14, 15c Tip processus transpalatinus with the number of measurements available
16, 17c Angulus caudolateralis of palatine for a particular landmark (maximum N=7).
18, 19c Connection palatineupper beak The overall s.d. after convergence for a
20 Lateral position of connection jugalupper beak
stationary point was 0.052 mm (d.f.=705).
21, 22c Ventral position of connection jugalupper beak
23 Base processus postorbitalis
However, after convergence the (pooled)
24 Tip processus postorbitalis s.d. for the rotating points was clearly
25 Base processus zygomaticus higher. With an average number (3.9) of
26 Tip processus zygomaticus photographs showing a particular
27 Most dorsolateral point processus paroccipitalis landmark, the standard error for the
28, 29c Most ventral point processus paroccipitalis average x and y estimated is approximately
30 Condylus occipitalis
31 Most caudal point cranium
0.1 mm.
32 Most rostromedial point vomer
33 Most medial connection between quadrate and skull (capitulum squamosum quadrati) Morphometrics
Shape analysis was performed after a
c, measured on contralateral side.
Generalised Procrustes Analysis (GPA) as
Distance (mm)
2
(Rohlf, 2004)]. 2 6
Univariate relationships between distances between landmarks 8
and body mass were directly calculated from the 3D measurements. 0 3
These distances were analyzed with the standardized major axis
2 1 5
routine (S)MATR (v1) (Falster et al., 2003). This routine implements 4
the algorithms developed by Warton and Weber (Warton and Weber, 4 7
2002).
6
Static bite force model 8
In order to determine the extent to which the differences in the shape
5 0 5 10
of the skull between fringillids and estrildids result in differences
in maximal bite force, we used a 2D static bite force model. The Distance (mm)
model calculates the position of all muscles and the lower jaw for
a seed of a given diameter and at a given position in the beak, and Fig. 3. The 2-D model of the avian skull, here illustrated by a spice finch
adapted from Nuijens and Zweers (Nuijens and Zweers, 1997). (A) The
finds the set of muscles force for which the bite force (force skeletal points (1-12; see Table 2) of the model. (B) The bars connecting
perpendicular to the upper beak) is maximal. the model points (grey) and the muscle groups (black). 1, Musculus
Although a large number of landmarks on the skull were depressor mandibulae; 2, musculus adductor mandibulae externus and
measured, only a limited number of points are directly related to musculus pseudotemporalis superficialis; 3, musculus protractor quadrati;
bite force (e.g. points defining the joints between neurocranium, 4, musculus protractor pterygoidei; 5, musculus pseudotemporalis
quadrate, pterygoid, palatine and the jaws). Nine landmarks were profundus and musculus adductor mandibulae ossis quadrati; 6, musculus
pterygoideus ventralis and musculus pterygoideus dorsalis pars lateralis (all
used in the static force model and define the basic framework of
muscle fibre groups attached to the palatine); 7, musculus pterygoideus
the skull. Variation in their position may affect bite force directly. dorsalis pars medialis (muscle fibres attached to the pterygoid); 8,
In the 2D model the joints between the bony elements of the skull musculus retractor palatini. Axis labels represent distance of markers and
are defined by x and y coordinates from the morphometric analysis muscles from centre of skull.
(Fig. 3A; Table 2).
The jaw muscles were divided into eight groups, which are
illustrated in Fig. 3B. For an extensive description of the jaw muscles muscle groups according to the average percentage for each jaw
in estrildids and fringillids see Nuijens and Zweers (Nuijens and muscle group as calculated from previously published data (van der
Zweers, 1997). Meij and Bout, 2004). Maximal forces were estimated by scaling
The maximal force of jaw muscles was calculated from the muscle down the fibre length for each muscle group measured in the
mass and fibre length using the formula: greenfinch, using the relationship between centroid size and adductor
fibre length (see van der Meij and Bout, 2004).
Fmax = m / (l)Mc ,
To remove the medially directed muscle force components for
where Fmax=maximal muscle force (N); m=muscle mass (kg); the 2D model a 3D analysis of directions of jaw muscles was made
l=mean fibre length (m); =muscle density (1000kgm3); Mc=muscle for the greenfinch by measuring the coordinates of the origin and
stress constant [330 N m2 (Hildebrand et al., 1985)]. insertion of all muscle groups (same procedure as for the landmarks
Data on the xy coordinates of origin and insertion of muscles and of the skull). The orientations of the muscles of the greenfinch were
muscle mass were not available for all species. We therefore fitted to the average skull by scaling the greenfinch down to the
estimated maximal muscle forces and muscle orientation for an centroid size of the average skull and then the landmarks of the
average skull from the data of the morphometric analysis. greenfinch skull were least-squares fitted to the landmarks of the
Jaw muscle weights for the average skull were calculated using average skull. After estimating the maximal bite force for the whole
the regression between total jaw muscle weight and centroid size. muscle the force components in the xy plane of the 2D static force
The estimated total jaw muscle weight was divided over the eight model were calculated. The orientation and maximal force of all
muscles were kept constant for all calculations involving skull shape RESULTS
comparisons. Shape analysis
The virtual seed (2 mm diameter) was positioned near the corner The mean skull configurations of a selected number of landmarks
of the mouth (rictus=0) at 20% of the distance to the beak tip (=1). for fringillids and estrildids after Procrustes superimposition are
This position was roughly estimated from video recordings of birds shown in Fig. 4. The differences between landmarks for the average
trying to crack relatively hard seeds. The diameter going through skull size of the two groups are between 0 and 0.6 mm. The variation
the centre of the seed and the point where the seed touches the upper between groups is much smaller than the variation within groups.
beak was kept perpendicular to the line defining the rim of the upper Differences in landmark coordinates within groups vary between
beak. 0.5 and 3.5 mm.
Finches have the ability to move their upper jaw relative to the Our data set consisted of more variables (33 points in 3D=99)
braincase [prokinesis (Bock, 1964; Bhler, 1981; Zusi, 1984; than species (N=42), so it was not possible to test the effect of size
Gussekloo et al., 2001)]. A somewhat different version of the static and family on shape directly. To reduce the dimensionality a
force model used to calculate bite force in the spice finch showed principal component analysis (PCA) was performed on the
that bite force is slightly higher with elevated upper beak than with variancecovariance matrix of the Procrustes-fitted coordinates of
the upper beak in the resting position (Bout, 2002). This was not all the species. The PCA allowed us to take into account the
the case in our constructed average finch. All bite forces were correlation among coordinates of landmarks. The effects of group
therefore calculated with the upper beak in the resting position. (estrildid vs fringillid) and body size (3D centroid size) were tested
Bite forces were calculated under the assumption that muscles by a multivariate GLM over the first 17 principal components (PCs)
on both sides contribute to bite force. This was verified by EMG of the 3D data, which retained 90% of the shape variance. Both
recordings. factors were highly significant (group: F17,23=12.60, P=6.97108;
centroid size: F17,23=17.96, P=2.03109). Most of the variation
Electromyography (EMG) related to group and centroid size is described by the first three PCs,
To verify model assumptions, the jaw muscle activity patterns which explain 26.4%, 13.7% and 9.6% of the total shape variation,
(determined by EMG) during seed cracking were recorded in 11 respectively (total 49.7%). Subsequent PCs are mostly related to
Java sparrows. The birds were placed in a small box and kept under differences between species.
a steady flow of 0.3 l min1 medicinal oxygen, and 0.4 l min1 N2O As we intend to relate shape differences to bite force through a
with 1.8 vol% isofluothane. After approximately 30 min the birds 2D static bite force model we repeated the analysis with just the xy
were transferred to the operating table. During the operation the coordinates. The results of the 2D analysis were very similar to the
gaseous mixture was administered through a plastic tube inserted 3D results. The components of the 2D PCA were used as input for
into the beak and the amount of isofluothane was increased to 2.0 the bite force model.
vol%. Bipolar measurements of muscle activity were made using
eight 50 m twisted, copper wire electrodes, positioned four on the Principal components
left and four on the right side of each bird. For further details on The overall shape change of the skull was visualized through a thin
the operation and the electromyography, we refer to Nuijens et al. plate spline analysis (Fig. 5). For the parameters chosen (all principal
(Nuijens et al., 1997). To measure the gape a magnetoresistive sensor warps included and given the same weight) this analysis is equivalent
(Philips KMZ10B, Eindhoven, The Netherlands) was glued on the to a PCA of the Procrustes-fitted landmark coordinates.
upper bill. Opposite to the chip a small magnet was glued on the The first PC (or so-called relative warp) shows variation in the
lower bill. expansion of the area in front of the quadrate, in the dorsoventral
After recovery from the operation the birds were offered hemp position of the kinetic hinge of the upper beak and the orbit, and
seeds. During feeding the EMG signals were recorded with a 14- variation in the length of the neurocranium behind the quadrate
channel FM recorder [SE 700 tape recorder, S.E. Labs (EMI) Ltd., (Fig. 5A). This variation in shape is related to differences in body
Feitham, UK] and stored on Ampex tape with a speed of size. The factor scores of PC1 are negatively correlated with 2D-
18.75 cm s1. The EMG signals were amplified 1000 times and high- centroid size for both estrildids (r=0.686, N=22, P=0.000) and
pass filtered at 50 Hz. fringillids (r=0.814, N=20, P=0.000). Standardized major axis
After the experiments, the birds were sacrificed by an overdose analysis shows that the slope (P=0.535) and intercept (P=0.070) of
of Nembutal, and the position of the electrodes was determined by the relationship between factor scores and centroid size is similar
dissection. The jaw muscles were divided into eight groups (see for the two groups of finches (Fig. 6, PC1).
static bite force model section). For all groups the muscle activation
patterns of one or more muscles were recorded, except for the very 12
small M. retractor palatini. For EMG analysis the data were 10
simultaneously digitized at a sample rate of 5000 Hz. 8
Distance (mm)
12
1 10 PC1
8
6
0 4
2
0
1
2
4
2 0 2 4 6 8 10 12 14 16 18 20
12 PC2
3 PC1 10
Distance (mm)
8
30 40 50
6
4 PC2 4
2
3 0
2
Bartlett factor score
4
2
0 5 10 15 20
1
12
10 PC3
0
8
6
1
4
2 2
0
20 30 40 50 60 2
4
3
0 2 4 6 8 10 12 14 16 18 20
2 Distance (mm)
Fig. 7. The effect of the first three principal components (PC13) on the
1 configuration of skull landmarks used for the static force model. The
configuration of the skull in the positive direction is represented in black, in
0 the negative direction in grey. The change has the same magnitude for
each PC and does not represent the measured variation but was chosen
for graphical purposes only. Axis labels represent distances with respect to
1
the centroid of the measured skull points.
The variation in bite force associated with the shape changes Table 4. The effect on bite force of the first three principal
described by PC3 is slightly more complex. With increasing components describing shape variation in estrildids and fringillids
head/body size the relative length of the beak increases, the height Bite force (N) for PC-length
of the frontonasal hinge decreases, and the quadrate shifts caudally.
3 +3
These shape changes increase bite force (Table 4). Part of the
increase in bite force comes from the caudal shift of the quadrate, PC1 12.5 10.4
as in PC1. The other part comes from the shortening of the palatine PC2 10.7 12.6
PC3 12.4 11.3
and jugal.
When the seed is kept in the same position as in an average finch,
changing the position of the beak tip has no effect on bite force.
The position of the connection of the jugal with the upper beak, 1966). Without a biomechanical analysis, however, interpretations
however, does have an effect. In finches the position of this of changes in shape of the skull remain hazardous, because
connection is indicative of the position of the corner of the mouth differences in skull morphology may not only be related to variation
(rictus). There is a high correlation between the external length of in bite force, but also to variation in the attachment area for jaw
the beak of the intact animal measured between rictus and beak tip, muscles or to differences in the resistance to joint reaction forces,
and the length of the beak measured on the skull between the or could be the consequence of changes in the shape or position of
connection jugalupper beak and beak tip (r=0.945, N=19). When neighboring structures.
palatine and jugal become shorter but the position of the seed remains
unchanged bite force becomes lower. However, when the rictus Skull configuration and maximal bite force
moves caudally with the connection between jugal and upper beak, The analysis of the relationship between the position of landmarks
the seed may also move caudally to stay at the same (absolute) and bite force suggests that only a few changes are directly related
distance to the rictus. When the seed also moves caudally bite force to bite force. Most differences in landmarks that are present in the
increases strongly. static force model result in small changes in bite force, and only
three characters have a large impact on bite force: a caudal shift of
EMG the quadrate (PC1), a downward inclination of the beak (PC2) and
A representative example of the EMG activity of a number of jaw a caudal shift of the rictus (PC3).
muscles during seed cracking is shown in Fig. 8. There is no Lengthening of the quadrate leaving its orientation and all
difference between EMG activity during successful and unsuccessful muscles unchanged by itself does not increase bite force, but a more
cracking attempts (not shown here). Muscles on the right side and caudal position of the quadrate does increase the lever arm of jaw
left side of the bird show very similar activation patterns. closer muscles. Large billed Geospizinae species also have a more
A cracking attempt starts with a very small amplitude closing posterior position of the quadrate than small-billed species
movement (vertical line 1 in Fig. 8), followed by re-opening before (Bowman, 1961). However, the increase in lever arm is not
the actual cracking starts (vertical line 2 in Fig. 8). During re-opening independent of muscle size. The expansion of the area around the
only the upper and lower jaw openers are active. When jaw opener quadrate with increasing head/body size (PC1) is related to the
activity decreases the jaws start to close for the actual cracking positive allometric increase of jaw muscle size with body size. The
attempt starts. During the cracking attempt the adductors inserting processus zygomaticus and processus orbitalis of the quadrate serve
on the quadrate, the adductors of the lower jaw and the pterygoid as (musculous) attachment area for jaw closer muscles, while a
muscles are all active. The amplitude of the muscle activity increases large part of the upper jaw closers attach to the pterygoid and to
until the seed cracks or until the cracking attempt is terminated. the transpalatine process. Jaw muscle mass increases so fast with
When adductor and pterygoid activity decreases the jaws start to body size (body mass1.29) that the linear dimensions of attachment
open again (vertical line 3 in Fig. 8). There is some low level activity areas have to increase with an exponent of 0.43. As a result of the
of the protractor of the quadrate (upper jaw openers) during a positive allometric increase of skull dimensions in the jaw closer
cracking attempt. attachment area, the processus orbitalis becomes longer and the
quadrate shifts backwards. This leaves the origo and insertion of
DISCUSSION the quadrate adductors approximately the same and increases the
Fringillids and estrildids differ in their husking performance on hard lever arm of the quadrate adductors. The increase in skull
closed-shelled seeds. The time required to crack a seed is directly dimensions around the quadrate also affects the position of the
related to seed hardness and to maximal bite force (van der Meij et processi zygometicus and postorbitalis. These processi, which
al., 2004; van der Meij and Bout, 2006). In a previous study (van border the orbit, move upwards. Consequently, when the diameter
der Meij and Bout, 2004) we showed that there is a significant of the eye and orbit has to remain the same, the orbit has to move
difference in jaw muscle mass and maximal bite force between upward too.
fringillids and estrildids. Fringillids have relatively larger jaw The increase in the area for muscle attachment does not seem to
muscles than estrildids and are able to produce higher bite forces affect skull width. The distances between left and right processus
than estrildids of the same body size. Compared to other birds the paroccipitalis just behind the ear and between the left and right
jaw muscles of both fringillids and estrildids scale positively quadratopterygoid joints increase isometrically (Table 3). A strong
allometrically with body size. relationship between head width and bite force has been found in
Differences in maximal bite force within and between taxa may Darwins finches (Herrel et al., 2005b). However, we did not find
depend not only on differences in jaw muscle forces, but also on any difference in skull width between fringillids and estrildids. As
differences in the geometry of the cranial elements that affect lever the external head measurements in Darwins finches include the
arms. A high upper bill (kinetic hinge), for instance, is often voluminous jaw muscles, differences in relative head width as found
interpreted as an adaptation to large bite force because it increases in Darwins finches may reflect differences in relative jaw muscle
the moment of the upper jaw closing muscles (Bowman, 1961; Bock, size (and therefore bite force) rather than differences in skull width.
ventralis.
0
3
r.Ps
0
rictus to create a shorter work arm for the jaw
0.1
closer muscles. This is especially clear in large
1 2 3 fringillids (Eophona, Coccothraustes,
Time Mycerobas). Although variation in the position
of the connections of jugal and palatine with
the upper beak does occur, this variation is
The change in bite force that is associated with PC2 is largely limited, possibly by spatial constraints. In finches the distance
the result of the change in angle between the beak and the skull. In between the beak and eye is much smaller than in many other
estrildids the beak becomes much more inclined downward with species. A large decrease in the distance between beak and the jaw
increasing skull size (e.g. Pyrenestes sanguineus) than in fringillids. closing muscles to get a shorter work arm with increasing body size
The increase in bite force with a more downward inclined beak is may not be possible because the eye and muscles occupy all the
caused by the small decrease in distance between the seed and the space between the beak and quadrate. In estrildids there is no
jaw muscles. Why the downward inclination of the beak is so much significant correlation between the position of the connections
more pronounced in estrildids than in fringillids is not clear. between jugal and palatine with the upper beak (PC3) and head/body
Increasing jaw muscle mass (see below) may be much more size. Unfortunately, the range of body mass in estrildids is limited
effective for increasing bite force than shape changes of the skull. because, unlike fringillids, there are no estrildids with a body mass
Alternatively, an increase in jaw muscle mass may be constrained over 40 g. This makes it difficult to establish the relationship with
in estrildids and shape changes may be the only option to increase certainty. The larger variation in the position of jugal and palatine
bite force. connections with the upper beak in fringillids may represent species-
specific shape differences and not be related to differences between estimated. Although muscle orientation seems very similar across
the two groups of finches. species, small changes in muscle orientation may have a large effect
on bite force.
Other landmarks For the calculation of maximal muscle forces it is assumed that
Contributions to bite force from the variation of other landmarks, the muscles on both sides of the head contribute to bite force. The
e.g. a dorsal shift of the frontonasal hinge, are not only relatively EMG recordings show that left and right jaw muscles are
small compared to the effect of the main shape changes, but also approximately active at the same time and with the same amplitude
covary with changes in landmarks that effect bite force negatively. during cracking. This muscle activation pattern is in good agreement
The relatively small contribution of some of the landmarks is not with the results predicted by the model for maximal bite force. Low-
just because the observed changes differ in magnitude. Lowering level activity of the protractor muscles in the model critically
the beak tip or raising the frontonasal hinge over the same distance, depends on the position of the seed along the beak but is also
for instance, shows that changing the position of the frontonasal predicted for submaximal bite forces. The activity of the very small
hinge is far less effective than changing the angle of the beak. The retractor palatini could not be verified.
covariation of differences in landmarks that affect bite force
positively or negatively is surprising because when there is a strong Differences between fringillids and estrildids
selection on large bite force one would not expect to find shape The analysis of landmarks representing the basic shape of the skull
changes that contribute to a decrease in bite force. This makes it shows that, although there are small but significant differences
difficult to understand the functional significance of an increase in between some of the landmarks, the difference between the two
bill height (frontonasal hinge). In finches the cranium is relatively families is small compared to interspecific variation. The relationship
short compared to many other birds with relatively smaller jaw between log jaw muscle mass and log bite force for the two taxa
muscles (e.g. anseriformes, unpublished observations) and the described previously (van der Meij and Bout, 2004) already explains
frontonasal hinge directly borders the dorsoanterior part of the orbit. 88% of the variation in bite force. Most of the total variation in
In many other species the frontonasal hinge is more in front of the skull geometry (approximately 78%) represents differences in size,
orbit. The position of the frontonasal hinge close to the orbit which leaves very little variation in bite force to be explained by
suggests that the hinge may shift upward with the orbit as a differences in shape between the two groups of finches.
consequence of the expansion of the jaw closer attachment area. Static bite force calculations show that the effect of the difference
An increase in bite force is not always associated with a higher in average shape between fringillids and estrildids is small. An
beak (PC1). In PC3 an increase in bite force is associated with a average fringillid skull has a slightly higher bite force (0.5 N) than
more ventrally positioned hinge. Alternatively, variation in the an average estrildid skull for the same muscle sizes and
height of the frontonasal hinge may be related to the reaction force configuration. This difference is very small compared to the effect
in the hinge. Model calculations show that the reaction force in the of the smaller jaw muscle mass in estrildids (van der Meij and Bout,
hinge decreases for the same bite force as its height increases. As 2004). Jaw muscle mass is approximately 0.67 times lower in
finches evolve stronger jaw muscles and larger bite forces, estrildids than in fringillids of the same size. For the calculated
corresponding changes in beak height may be required to avoid maximal bite force of the average estrildid in the present study this
structural failure of the very thin flexible zone of the kinetic hinge amounts to a decrease in bite force of approximately 4.0 N.
(see also Herrel et al., 2005b). The comparison of bite force between the average skull
A similar explanation may hold for the changes in the configurations of the two taxa, however, is biased because the
pterygoid/palatine chain that are associated with a more caudal fringillids in our samples are larger than the estrildids. When the
position of the quadrate with increasing head size (PC1). The three largest fringillids are removed (Mycerobas, Coccothraustes,
combined effect on bite force of the relative shortening of the Eophona) to make average body weight comparable, the caudal shift
palatine, a more dorsal position of the palatine, and the more ventral of the quadrate and the connection between jugal and upper beak
position of the quadratepterygoid joint is negligible, but the disappear. Surprisingly, the shape of the unbiased average fringillid
reaction forces in the perygoidpalatine joint, the quadratepterygoid skull is less suited to generate bite force than the shape of the average
joint and the connections of the jugal all become relatively smaller, estrildid skull: bite force is lower (11.1 vs 11.9 N) for the fringillid
compared to a model skull with just a more caudally positioned skull than for the estrildid skull. The higher bite force of the estrildid
quadrate. The reaction force in the connection between palatine and skull is almost completely the result of the more depressed angle
upper beak, on the other hand, increases. of the bill. For an average estrildid skull with the beak elevated to
Interestingly, the shape changes in the pterygoidpalatine chain the same position as in the average fringillid the bite force is 1.0 N
associated with the more posterior position of the quadrate (PC1) lower.
are partly reversed in PC2: the quadratepterygoid joint is positioned The frontal nasal hinge has a more rostral position in fringillids
more dorsally, and the palatine becomes relatively longer. This than in estrildids. The difference is small (0.6 mm) and model
increases joint reaction forces in estrildids (see before) compared calculations show that this difference contributes very little to
to fringillids when bite force is the same, but jaw muscles and bite force. Similarly, the small differences in the position of the
maximal bite force are systematically smaller in estrildids than in joint between the pterygoid and the quadrate, the connection
fringillids. Therefore, reaction forces may in fact be similar for birds between the pterygoid and palatine, and the connection between
of the same size. the jugal bar and the quadrate contribute very little to bite force.
Many other differences between the two groups of finches do not
Model calculations and EMG contribute to bite force directly, but only indirectly through the
To assess differences in skull shape the size and orientation of positive allometric growth of the jaw muscles (e.g. the length and
muscles is kept constant in the model. Whether there are differences position of processi serving as attachment area), or may be related
in muscle orientation between taxa was not investigated as the to the consequences of large bite forces or to the way seeds are
centres of origin and insertion of muscles may only be roughly cracked.
Several studies have shown that bite force is correlated with beak Abbott, I., Abbott, L. K. and Grant, P. R. (1977). Comparative ecology of Galapagos
ground finches (Geospiza Gould): evaluation of the importance of floristic diversity
height and width (Herrel et al., 2005b), and that there are and interspecific competition. Ecol. Monogr. 47, 151-184.
performance and fitness advantages for birds with deep and wide Abzhanov, A., Kuo, W. P., Hartmann, C., Grant, B. R., Grant, P. R. and Tabin, C.
J. (2006). The calmodulin pathway and evolution of elongated beak morphology in
beaks in cracking hard seeds (Grant and Grant, 1995; Grant and Darwins finches. Nature 442, 563-567.
Grant, 1999; Benkman, 2003). In our study a strong positive Arnold, S. J. (1991). Constraints on phenotypic evolution. Am. Nat. 140S, 85-107.
Beach, J., Gomiak, G. C. and Gans, C. (1982). A method for quantifying
allometric increase in jaw muscle mass and bite force with body electromyograms. J. Biomech. 15, 611-617.
mass (Van der Meij and Bout, 2004) is associated with a positive Benkman, C. W. (1993). Adaptation to single resources and the evolution of Crossbill
allometric increase in both height and width of the beak in both (Loxia) diversity. Ecol. Monogr. 63, 305-325.
Benkman, C. W. (2003). Divergent evolution drives the adaptive radiation of
groups of finches. Bite force in estrildids is only 71% of similar Crossbills. Evolution 57, 1176-1181.
sized fringillids and one would therefore expect the relatively large Bjrklund, M. (1991). Patterns of morphological variation among cardueline finches
(Fringillidae: Carduelinae). Biol. J. Linn. Soc. Lond. 43, 239-248.
difference in bite force to be reflected in differences in beak height Bjrklund, M. and Meril, J. (1993). Morphological differentiation in Carduelis finches:
and width. Beak height, however, is only close to significance, adaptive vs. constraint models. J. Evol. Biol. 6, 359-373.
Boag, P. T. and Grant, P. R. (1981). Intense natural selection in a population of
possibly because the range of body sizes of the birds in this study Darwins finches (Geospizinae) in the Galapagos. Science 214, 82-85.
is small. Beak width measured as the distance between the Bock, W. J. (1964). Kinetics of the avian skull. J. Morphol. 114, 1-42.
Bock, W. J. (1966). An approach to the functional analysis of the bill shape. Auk 83,
connections of jugal and upper beak is not different for the two 10-51.
groups of finches. Beak width measured externally, including the Bookstein, F. L. (1991). Morphometric Tools for Landmark Data: Geometry and
Biology. New York: Cambridge University Press.
ramphotheca, on the other hand is clearly different. Apparently, the Bout, R. G. (2002). Biomechanics of the avian skull. In Vertebrate Biomechanics and
width of the ramphotheca is larger in fringillids than in estrildids. Evolution (ed. V. L. Bels, J.-P. Gasc and A. Casinos), pp. 229-242. Towbridge:
Cromwell Press.
Larger bite forces in fringillids allow birds to crack harder seeds. Bowman, R. I. (1961). Morphological Differentiation and Adaptations in the Galapagos
As seed hardness and seed size are correlated (Abbott et al., 1977; Finches. Berkeley: University of California Publications in Zoology.
Bhler, P. (1981). The functional anatomy of the avian jaw apparatus. In Form and
Van der Meij and Bout, 2000) one would expect a wider husking Function in Birds. Vol. 2 (ed. A. S. King and J. McLelland), pp. 439-468. London:
groove in the ramphotheca of fringillids to efficiently crack the larger Academic Press.
seeds (Benkman, 1993; Benkman, 2003). Bunday, B. D. (1984). Basic Optimisation Methods. London: Edward Arnold.
Daz, M. (1990). Interspecific patterns of seed selection among granivorous
Both height and length of the bill increase positively allometrically passerines: effects of seed size, seed nutritive value and bird morphology. Ibis 132,
with body size and tend to be larger is estrildids than in fringillids, 467-476.
Falster, D. S., Warton, D. I. and Wright, I. J. (2003). (S)MATR: standardised major
but there is a large variation within the two groups. It has been axis tests and routines. Version 1.0. http://www.bio.mq.edu.au/ecology/SMATR.
shown that beak length is controlled independently from beak height Grant, P. R. (1986). Ecology and Evolution of Darwins Finches. Princeton, NJ:
Princeton University Press.
and width during development (Abzhanov et al., 2006). Grant, B. R. and Grant, P. R. (1989). Evolutionary Dynamics of a Natural Population:
In fringillids the distance between the lateral and medial condyle The Large Cactus Finch of the Galapagos. Chicago: University of Chicago Press.
Grant, P. R. and Grant, B. R. (1995). Predicting microevolutionary responses to
of the joint between the quadrate and mandible is larger than in directional selection on heritable variation. Evolution 49, 241-251.
estrildids. This increases the articular surface of the quadrate with Gussekloo, S. W. S., Vosselman, M. G. and Bout, R. G. (2001). Three dimensional
kinematics of skeletal elements in avian prokinetic and rhynchokinetic skulls
the mandible and may be an adaptation to large compression forces determined by roetgen stereophotogrammetry. J. Exp. Biol. 204, 1735-1744.
in the quadratomandibular joint (Bowman, 1961). A broad Hammer, ., Harper, D. A. T. and Ryan, P. D. (2001). PAST: paleontological
statistics software package for education and data analysis. Palaeontol. Electronica
quadratomandibular joint may also contribute to stability of the joint 4, 1-9.
during powerful adduction (Bowman, 1961) or be related to the large Herrel, A., Podos, J., Huber, S. K. and Hendry, A. P. (2005a). Bite performance and
morphology in a population of Darwins finches: implications for the evolution of beak
lateral lower jaw movements during seed handling in fringillids, shape. Funct. Ecol. 19, 43-48.
which are absent in estrildids (Ziswiler, 1965; Abbott et al., 1975; Herrel, A., Podos, J., Huber, S. K. and Hendry, A. P. (2005b). Evolution of bite force
in Darwins finches: a key role for head width. J. Evol. Biol. 18, 669-675.
van der Meij and Bout, 2006). Hespenheide, H. A. (1966). The selection of seed size by finches. Wilson Bull. 78,
In summary we conclude that most morphological variation 191-197.
related to bite force among the granivorous species of the Fringillidae Hildebrand, M., Bramble, D. M., Liem, K. F. and Wake, D. B. (ed.) (1985).
Functional Vertebrate Morphology. Cambridge, MA: Harvard University Press.
and Estrildidae is confined to size. As bite force is largely determined Kear, J. (1962). Food selection in finches with special reference to interspecific
by jaw muscle size and jaw muscles scale positively allometrically differences. Proc. Zool. Soc. Lond. B 138, 163-204.
Meril, J. and Bjrklund, M. (1999). Population divergence and morphometric
with body size in both groups, selection for high bite force more or integration in the greenfinch (Carduelis chloris) evolution against trajectory of least
less coincides with selection for body size. resistance. J. Evol. Biol. 12, 103-112.
Nuijens, F. W. and Zweers, G. A. (1997). Characters discriminating two seed husking
The contribution of variation in shape to bite force is modest, mechanisms in finches (Fringillidae: Carduelinae) and (Passeridae: Estrildinae). J.
largely size dependent and similar in estrildids and fringillids. Only Morphol. 232, 1-33.
Nuijens, F. W., Snelderwaard, P. C. and Bout, R. G. (1997). An electromyographic
one character clearly contributes to the difference in bite force technique for small animals. J. Neurosci. Methods 76, 71-73.
independent of size: the angle of depression of the bill. The bill is Raikow, R. J. (1977). The origin and evolution of the Hawaiian honeycreepers
(Drepanididae). Living Bird 15, 95-117.
inclined downward more in estrildids than in fringillids. This shape Read, J. L. (1991). Consumption of seeds by Red-browed Firetails Neochmia
difference results in a slightly higher bite force but does not temporalis at feeders: dehusking rates and seed choice. Corella 15, 19-23.
Rohlf, F. J. (1998). TpsSmall, version 1.20. Department of Ecology and Evolution,
compensate for the much smaller jaw muscle size in estrildids. The State University of New York at Stony Brook, http://life.bio.sunysb.edu/morph.
variation in the position of other landmarks is related to muscle size Rohlf, F. J. (2004). TpsRelw, version 1.40. Department of Ecology and Evolution,
State University of New York at Stony Brook, http://life.bio.sunysb.edu/morph.
or may be related to the reduction of reaction forces in the jaw Rohlf, F. J. and Slice, D. E. (1990). Extensions of the Procrustes method for the
apparatus. optimal superimposition of landmarks. Syst. Zool. 39, 40-59.
Schluter, D. (1982). Seed and patch selection by Galapagos ground finches: relation
to foraging efficiency and food supply. Ecology 63, 1106-1120.
We wish to thank Wouter van Gestel from Wageningen University for help with Schluter, D. and Smith, N. M. (1986). Natural selection on beak and body size in the
collecting the species and M. Heijmans of the technical department of our institute song sparrow. Evolution 40, 221-231.
for constructing the rotating device. Sibley, C. G. and Monroe, B. L. (1990). Distribution and Taxonomy of Birds of the
World. New Haven: Yale University Press.
Sibley, C. G. and Monroe, B. L. (1993). Supplement to Distribution and Taxonomy of
REFERENCES Birds of the World. New Haven: Yale University Press.
Abbott, I., Abbott, L. K. and Grant, P. R. (1975). Seed selection and handling ability Smith, T. B. (1987). Bill size polymorphism and intraspecific niche utilization in an
of four species of Darwins finches. Condor 77, 332-335. African finch. Nature 329, 717-719.
Smith, T. B. (1991). Inter- and intra-specific diet overlap during lean times between van der Meij, M. A. A., de Bakker, M. A. G. and Bout, R. G. (2005). A phylogeny of
Quelea erythrops and bill morphs of Pyrenestes ostrinus. Oikos 60, 76-82. finches and their relatives based on nuclear and mitochondrial DNA. Mol.
van der Meij, M. A. A. and Bout, R. G. (2000). Seed selection in the Java sparrow Phylogenet. Evol. 34, 97-105.
(Padda oryzivora): preference and mechanical constraint. Can. J. Zool. 78, 1668- Warton, D. I. and Weber, N. C. (2002). Common slope tests for bivariate errors-in-
1673. variables models. Biom. J. 44, 161-174.
van der Meij, M. A. A. and Bout, R. G. (2004). Scaling of jaw muscle size and Willson, M. F. (1971). Seed selection in some North American finches. Condor 73,
maximal bite force in finches. J. Exp. Biol. 207, 2745-2753. 415-429.
van der Meij, M. A. A. and Bout, R. G. (2006). Seed husking performance and Ziswiler, V. (1965). Zur kenntnis des Samenffnens und der Struktur des hrnernen
maximal bite force in finches. J. Exp. Biol. 209, 3329-3335. Gaumens bei krnerfressenden Oscines. J. Ornithol. 106, 1-47.
van der Meij, M. A. A., Griekspoor, M. and Bout, R. G. (2004). The effect of seed Zusi, R. L. (1984). A functional and evolutionary analysis of rhynchokinesis in birds.
hardness on husking time in finches. Anim. Biol. 54, 195-205. Smiths. Contrib. Zool. 395, 1-37.