|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 17, 2006
Journal of Experimental Biology 209, 3329-3335 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02379
Seed husking time 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: m.a.a.van.der.meij{at}biology.leidenuniv.nl)
Accepted 12 June 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In our experiments we measured the seed husking time and the maximal bite force of two taxa of seed cracking birds. Husking time is related to maximal bite force in a highly non-linear way and differs between estrildids and fringillids. Fringillids with the same bite force as estrildids take less time to crack seeds, but only when the strength of the seed coat is close to their maximal bite force. For seeds that are relatively soft the difference in husking time becomes very small. A preliminary jaw motion analysis provides evidence that this difference in husking time between estrildids and fringillids is paralleled by a difference in husking technique. This difference in technique does not affect bite force as such, but decreases the chance of failed cracking attempts.
The selective advantage of a small increase in maximal bite force may be related more to the decrease in husking time for seeds with hardness below the maximal bite force, than to the increase in range of seed hardness that the bird is able to crack.
Key words: bite force, feeding performance, seed hardness, jaw movement, finches
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Grant and Grant, 1989).
Variation in food availability and interspecific competition result in natural
selection for specific feeding habits and beak morphologies
(Grant, 1986). Within species
variation in beak size has been directly related to differences in the
selection of different proportions of the available range of seed sizes
(Grant et al., 1976; Abbot et
al., 1977; Boag and Grant,
1984; Grant and Grant,
1996).
Most studies on the efficiency of feeding in finches concentrate on husking
time in relation to average seed size and bird size
(Kear, 1962;
Hespenheide, 1966; Willson,
1971; Schluter, 1982;
Diaz, 1990;
Read, 1991). Large species are
capable of eating larger seed species and are able to husk large seeds faster
than smaller species. Benkman and Pulliam
(Benkman and Pulliam, 1988)
demonstrated that cardueline finches are not only much faster handling large
seeds than emberizine sparrows of the same body size, but also eat a wider
range of seed sizes. An increase in the range of a diet with increasing bite
force has been reported for a number of vertebrates
(Wainwright, 1991;
Herrel et al., 1996;
Verwaijen, 2002;
Aguirre et al., 2003). As seed
size is correlated with seed hardness
(Abbott et al., 1977;
Van der Meij and Bout, 2000)
it is generally assumed that husking time is related to seed hardness and bite
force. However, there are very few studies that investigated the relationship
between husking time and seed hardness. Feeding time in two morphs of
Pyrenestes ostrinus is longer on plant species with large, hard seeds
than for species with small, soft seeds
(Smith, 1987), and husking
time decreases when hardness is experimentally lowered for the same seed
species (Van der Meij et al.,
2004).
Just as only a few studies directly investigate the relationship between
husking time and seed hardness, the number of studies that measure bite force
in birds is limited. Van der Meij and Bout
(Van der Meij and Bout, 2004)
and Herrel et al. (Herrel et al.,
2005a; Herrel et al.,
2005b) related bite force to head morphology. In Galápagos
finches bite force is not only related to beak size but even more strongly to
head width. Such a relationship may be expected since maximal bite force is
closely related to the size of the jaw adductor muscles
(Van der Meij and Bout, 2004)
and head size closely correlates with jaw muscle size
(Herrel et al., 2001;
Herrel et al., 2002).
In this study we investigate whether bite force is directly related to husking time in two groups of finches, the estrildids (Estrildidae) and fringillids (Fringillidae). From a previous study with various seed species we know that differences in husking performance between these two groups of finches do occur (R.B., personal observation). In the study reported here we offered a single seed species to a number of different species of both families, and husking times are related to bite force measurements of the same individuals.
Bite force is influenced by the geometry of the skull and jaw muscles, and
the size of the jaw closing muscles. The effect of differences in skull
geometry between estrildids and fringillids is relatively small compared to
the difference in muscle size (Van der
Meij and Bout, 2004). However, it is not clear whether the size of
the jaw muscles is the only factor determining husking time. Alternatively,
differences in husking time may be the result of differences in husking
technique. Ziswiler described two different techniques: crushing and cutting.
Estrildids use a crushing technique, whereas fringillids use a
forward/backward movement of the lower jaw (`cutting') during the cracking
phase (Ziswiler, 1965). We
therefore also performed a preliminary analysis of the cracking technique of
an estrildid and a fringillid.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
).
In contrast to so-called open-shelled seeds, in which the two husks envelop
the kernel only loosely, birds need to apply considerable force on the seed
before the husk splits into two parts. In open-shelled seeds the husks can be
removed very quickly without actually cracking the seed coat
(Kear, 1962). The mean
hardness of hemp seeds was 12.16±4.95 N. The hardness of the seeds was
measured by stepwise lowering of a force transducer pressing on individual
seeds, and recording the peak force at the point where the seed husk cracked
(see also Van der Meij and Bout,
2000).
|
Husking time measurements
All birds in the present study were purchased commercially and kept in the
laboratory in separate cages (40x38x38 cm) at 22°C and a 16
h:8 h L:D cycle. The food was removed from the cage the evening before the
experiments. The following day a large amount of hemp seeds (approximately
300) was offered to the birds. Trial experiments showed that the period of
food deprivation clearly affected husking time. To increase feeding motivation
and to measure maximal husking performance the period of food deprivation was
maximised and adjusted to the size of the species, i.e. between 20 h for the
largest species (Mycerobas affinis, 70 g) and 15 h for the smallest
species (Erythrura trichroa, 13 g). The seeds were offered in a small
transparent container hanging in front of the cage for 45 min. During this
time the bird was monitored with a standard video camera (25 frames
s-1). Husking time was determined from these recordings and taken
as the time from the moment a seed is picked up until the moment the first
half of the split husk fell out of the beak, with an accuracy of 0.04 s (1
frame).
|
Bite force
To measure the maximal bite force we used a force transducer (Aikoh, Osaka,
Japan; 9000 series) mounted with two flat metal plates
(Fig. 1). The birds were held
by hand and trained to bite the metal plates. The birds only used their beak
tips to bite the force transducer and refused to bite at more caudal positions
within the beak. Bite force measurements were performed several times in a row
at 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.
Jaw movements
To study the cracking technique high-speed video recordings (color
high-speed video; S-VHS; Nac, Beringen, Belgium, 250 fr s-1) of the
Java sparrow (estrildid) and the greenfinch (fringillid) were made. Up to 16
markers were placed on both sides of the bill and on top of the head. The
birds were offered hemp seeds on a small plateau surrounded by three mirrors
(left, right and overhead; Fig.
2) at an angle of 45° to the frontal plane. The co-ordinates
of markers on the head and of markers visible in the mirrors were digitised
and the three-dimensional (3D) position of the markers was reconstructed using
the direct linear transformation technique (DLT)
(Woltring and Huiskes, 1990).
The DLT transformation was based on a 3D-calibration object with 15 spherical
markers.
|
), was used. This routine implements the algorithms developed
by Warton and Weber (Warton and Weber,
2002).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Estrildids: husking time=1.43e8.56/bite force (R2=0.835)
Fringillids: husking time=1.83e5.09/bite force (R2=0.956)
The curves converge for high bite force to a theoretical minimum time necessary to crack a seed. This is the time necessary to process a seed with one single, successful cracking attempt. The minimum husking time is the same for the two families. Fringillids require a minimum time of 1.8 s to crack a hemp seed; the extrapolated prediction for estrildids is 1.4 s. From the baseline representing minimum husking time there is a rapid increase in husking time with decreasing bite force.
The survivorship analysis (Cox regression) on the husking times for all seeds, with family and maximal bite force as covariates gives similar results. There is a significant difference in husking time between estrildids and fringillids (P=0.002) as well as for different maximal bite forces (P=0.000). The estimated function for husking time is very similar to the one found for the model II regression on average husking time. The cumulative hazard function of the survival function estimates the change of a successful cracking attempt as a function of time. Fig. 4 shows that the chance that a hemp seed cracks within a certain amount of time is much higher in the fringillids than in the estrildids, irrespective of the difference in maximal bite force.
|
Seed cracking technique
In both the fringillids and the estrildids a seed is picked up and
transported to the back of the beak and placed between the rims of the beak.
This often requires only limited number (approx. 3) of beak movements. Once
the seed is placed correctly between the rims of the beak a cracking attempt
is made. This can be recognised by depression of the elevated upper jaw onto
the lower jaw. If the cracking attempt is successful part of the split husk
becomes visible at the outside of the beak. If the cracking attempt was not
successful the seed is repositioned between the rims and another attempt is
made. The preliminary analysis of the cracking technique shows that the lower
jaw makes a lateral movement just before a cracking attempt. During this
movement the tip of the lower jaw moves in a direction opposite to the side
where the seed is cracked. Its amplitude is much smaller in the Java sparrow
than in the greenfinch. In the Java sparrow the movement is about 1 mm,
whereas the movement of the lower jaw of the greenfinch is up to 4 mm
(Fig. 5). Note that in both
cases the amplitude of the movement is clearly larger than for the rigid upper
beak (measurement error).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Unlike the Darwin's finches in the study by Herrel et al.
(Herrel et al., 2005a;
Herrel et al., 2005b) the
birds in our study were not willing to bite the force transducer at a position
closely corresponding to that used to crack seeds. In most species the maximal
bite force measured at the tip of the beak is lower than the average hardness
of hemp, except in the greenfinch and the Chinese grosbeak. Static force
modelling (R.B., unpublished data) shows that maximal bite force increases
approximately linearly towards the base of the bill and is about two times
higher close to the rictus than at the tip of the beak. hemp seeds are usually
cracked about halfway between rictus and beak tip in species that easily eat
hemp, but are moved more caudally in species with a relatively low bite force.
In the smallest estrildids (e.g. Poephila, Lonchura) maximal bite
force is clearly less than the average hardness of hemp and only a small
amount of seeds at the lower end of the hardness range are available for the
birds. Note that this underestimates husking time in these species compared to
more powerful biters, because the average hardness of the seeds eaten is less.
The low number of husking times recorded in these species result from a lack
of motivation to continue searching for seeds that they are able to crack.
This mechanism of avoiding seed species that are too difficult to eat has been
reported in field studies as well (Newton,
1967) (see also Van der Meij
and Bout, 2000).
Husking time and bite force
Seed hardness together with maximal bite force determines which part of the
available food resources a bird is able to use. Species with a maximal bite
force that is higher than the seed hardness range are able to eat all seeds.
When maximal bite force falls within the range of seed hardness a bird will
also pick up seeds that are too hard to crack. Time spent handling seeds that
have to be rejected because they are too hard leads to a decrease in food
intake rate. High percentages of rejection of seeds occur in the field
(Grant, 1981;
Greig-Smith and Wilson, 1985).
Laboratory experiments with Java sparrows showed that birds do use size cues
as an indicator for seed hardness to avoid picking up seeds that are too hard
to crack, even when the correlation between seed size and hardness is very low
(Van der Meij and Bout, 2000).
Selective uptake of seeds has been reported for other species as well
(Hespenheide, 1966;
Willson, 1972).
Our data show that maximal bite force does not simply put an upper limit on
the hardness of the seeds that can be cracked and eaten, but that with
increasing bite force, less time is needed to crack seeds with hardness just
below the maximal bite force. This suggests that the selective advantage of a
small increase in maximal bite force may not only be related to the increase
in range of seed hardness available to the bird, but also to the decrease in
husking time for seeds with hardness just below the maximal bite force. Any
new seed available at the top of the range will require very large husking
times, while already available seeds just below the top of the hardness range
will be husked much faster than with a lower bite force. Which effect will be
more beneficial is not clear and may depend on the availability of seeds in
the environment. A similar relationship between maximal bite force and feeding
performance (handling time) may exist in lizards
(Verwaijen et al., 2002). The
increase in accessibility of seeds and faster husking times with increasing
bite force raises the question of why low bite force may be adaptive in some
species (cf. Grant et al.,
1976). Bite force increases positive allometrically with body mass
(Van der Meij and Bout, 2004).
However, large species seem to have problems manipulating relatively small
seeds and may have longer husking times on soft seeds than smaller species
with less bite force (M.A.A.M. and R.G.B., unpublished observation). This
would give small, less powerful biters an advantage over large species at the
low end of the range of accessible seeds. Whether this would also explain
differences in bite force between species of the same body size, for instance
because powerful biters have larger beaks, remains to be seen.
Seed cracking technique
Fringillids and estrildids differ in their husking time on hemp seeds,
independent of maximal bite force. Fringillids are on average faster than
estrildids, especially when their bite force is low (statistically when the
bite force is less than 7 N; see Fig.
3). Frame by frame analysis of a limited set of video recordings
of the seed cracking process in finches and estrildids showed that husking
time comprises two different phases (van
der Meij et al., 2004). During the transport phase, the seed is
transported to the back of the beak and positioned next to its rims. The
number of beak movements (mandibulations) required to transport a seed is the
same in finches and estrildids, and seems largely independent of seed size.
During the next phase the seed is manipulated to position it between the rims
of the beak. This often requires a number of small amplitude opening and
closing movements of the beak. Once the seed is positioned correctly, a
cracking attempt is made. If the cracking attempt fails, the whole process is
repeated until the cracking attempt is successful. The number of positioning
movements per cracking attempt increases with seed size, reflecting the
difficulty in manipulating large seeds. The number of cracking attempts
clearly increases with seed hardness and the largest contribution to
differences in husking time comes from the number of cracking attempts
(Van der Meij et al., 2004).
In birds that use a long time to crack a seed, many cracking attempts fail and
the seed is often squeezed from between the rims of the beak into the oral
cavity. The difference in husking time between estrildids and fringillids may
therefore be related a difference in the way the two groups handle the seed
during cracking attempts.
In a preliminary analysis we show that during a cracking attempt the tip of the lower jaw moves sideways from its medial position opposite the upper jaw, to a position left or right from the tip of the upper jaw. The amplitude of this mediolateral movement differs in the greenfinch, a fringillid, and in the Java sparrow, an estrildid. The mediolateral movement of the lower jaw is four times larger in the greenfinch than in the Java sparrow. Although the number of lower jaw movements analyzed was very limited, they may be representative for most movements, because the difference in amplitude is often clearly visible in video recordings.
|
). Crushing is
used by the estrildids and is characterised by opening and closing
(dorsoventral) movements of the jaws, restricted to the vertical plane.
Fringillids, however, are believed to use a forward/backward (rostrocaudal)
lower jaw movement (`cutting') during the cracking phase and mediolateral
movements of the lower jaw during the husking phase. A morphological analysis
of the jaw apparatus (Nuijens and Zweers,
1997) and our preliminary analysis of 3D kinematics of the lower
jaw suggest that the rostrocaudal movement may be an artefact of the 2D
analysis made by Ziswiler. In projection the large mediolateral movements of
the lower jaw present during seed cracking and husking in fringillids appear
to be `rostrocaudal' movements. We suggest that the lateral movement of the lower jaw does contribute to the shortening of husking time. When the lower beak is in its rest position it is not pressing against the centre of the seed, which is fixated in a groove of the upper beak, and there is a force component along the surface of the seed (Fig. 6A). When during a cracking attempt there is not enough friction between the lower beak and the seed, it is squeezed into the beak and another cracking attempt is needed. However, when the lower jaw moves in a lateral direction to a position right under the seed (Fig. 6B), the bite force is directed in such a way that chance of squeezing the seed from between the beaks becomes much smaller.
We have no reason to believe that the tongue plays a different role in the two groups of finches during seed cracking. It prevents the seed from falling into the beak in the same way that the most lateral ridge of the upper jaw prevents the seed from falling out of the beak. Lateral jaw movement may therefore decrease the number of cracking attempts and increases husking performance on closed-shelled seeds.
The difference in amplitude of lateral lower jaw movement between
estrildids and fringillids may be related to a difference in preferred seed
type. Estrildids are generally believed to feed mainly on open shelled seeds,
and remove the husks without actually cracking the seed coat
(Kear, 1962). Although the
force with which open-shelled seeds are dehusked cannot be measured directly
it is very probably low. Husking times for open-shelled seeds are low in
comparison to husking times for closed shelled seeds and very similar in
estrildids and fringillids of various sizes (R.G.B., personal observation).
Fringillids, on the other hand, feed primarily on closed-shelled seeds that
need to be cracked. As the number of failed cracking attempts may be expected
to be lower when biting forces are low, small amplitude lateral movements are
not necessary for species that feed mainly on open-shelled seeds.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
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 and interspecific competition. Ecol. Monogr. 47,151 -184.[CrossRef]
Aguirre, L. F., Herrel, A., Van Damme, R. and Matthysen, E. (2003). The implications of food hardness for diet in bats. Funct. Ecol. 17,201 -212.[CrossRef]
Benkman, C. W. and Pulliam, H. R. (1988). The comparative feeding rates of North American sparrows and finches. Ecology 69,1195 -1199.[CrossRef]
Boag, P. T. and Grant, P. R. (1984). The classical case of character release: Darwin's finches (Geospiza) on Isla Daphne Major, Galápagos. Biol. J. Linn. Soc. Lond. 22,243 -287.
Díaz, M. (1990). Interspecific patterns of seed selection among granivorous passerines: effects of seed size, seed nutritive value and bird morphology. Ibis 132,467 -476.
Falster, D. S., Warton, D. I. and Wright I. J. (2003). MATR: standardised major axis tests and routines. Version 1.0. http://www.bio.mq.edu.au/ecology/SMATR.
Grant, B. R. and Grant, P. R. (1989). Evolutionary Dynamics of a Natural Population. The Large Cactus Finch of the Galapagos. Chicago, London: The University of Chicago Press.
Grant, B. R. and Grant, P. R. (1996). High survival of Darwin's finch hybrids: effects of beak morphology and diets. Ecology 77,500 -509.[CrossRef]
Grant, P. R. (1981). The feeding of Darwin's finches on Tribulus cistoides (L.) seeds. Anim. Behav. 29,785 -793.[CrossRef]
Grant, P. R. (1986). Ecology and Evolution of Darwin's Finches. Princeton, NJ: Princeton University Press.
Grant, P. R., Grant, B. R., Smith, J. N. M., Abbott, I. J. and
Abbott, L. K. (1976). Darwin's finches: population variation
and natural selection. Proc. Natl. Acad. Sci. USA
73,257
-261.
Greig-Smith, P. W. and Wilson, M. F. (1985). Influences of seed size, nutrient composition and phenolic content on the preferences of bullfinches feeding in ash trees. Oikos 44, 47-54.
Herrel, A., Van Damme, R. and De Vree, F. (1996). Sexual dimorphism of head size in Podarcis hispanica atrata: testing the dietary divergence hypothesis by bite force analysis. Neth. J. Zool. 46,253 -262.
Herrel, A., Van Damme, R., Vanhooydonck, B. and De Vree, F. (2001). The implications of bite performance for diet in two species of lacertid lizards. Can. J. Zool. 79,662 -670.[CrossRef]
Herrel, A., O'Reilly, J. C. and Richmond, A. M. (2002). Evolution of bite force in turtles. J. Evol. Biol. 15,1083 -1094.[CrossRef]
Herrel, A., Podos, J., Huber, S. K. and Hendry, A. P. (2005a). Bite performance and morphology in a population of Darwin's finches: implications for the evolution of beak shape. Funct. Ecol. 19,43 -48.[CrossRef]
Herrel, A., Podos, J., Huber, S. K. and Hendry, A. P. (2005b). Evolution of bite force in Darwin's finches: a key role for head width. J. Evol. Biol. 18,669 -675.[CrossRef][Medline]
Hespenheide, H. A. (1966). The selection of seed size by finches. Wilson Bull.78,191 -197.
Kear, J. (1962). Food selection in finches with special reference to interspecific differences. Proc. Zool. Soc. 138,163 -204.
Newton, I. (1967). The adaptive radiation and feeding ecology of some British finches. Ibis 109, 33-98.
Nuijens, F. W. and Zweers, G. A. (1997). Characters discriminating two seed husking mechanisms in finches (Fringillidae: Carduelinae) and estrildids (Passeridae: Estrildinae). J. Morphol. 232,1 -33.[CrossRef]
Read, J. L. (1991). Consumption of seeds by red-browed firetails Neochmia teporalis at feeders: dehusking rates and seed choice. Corella 15, 19-23.
Schluter, D. (1982). Seed and patch selection by Galapagos ground finches: relation to foraging efficiency and food supply. Ecology 63,1106 -1120.[CrossRef]
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 Birds of the World. New Haven: Yale University Press.
Smith, T. B. (1987). Bill size polymorphism and intraspecific niche utilization in an African finch. Nature 329,717 -719.[CrossRef]
Van der Meij, M. A. A. and Bout, R. G. (2000). Seed selection in the Java sparrow (Padda oryzivora): preference and mechanical constraint. Can. J. Zool. 78,1668 -1673.[CrossRef]
Van der Meij, M. A. A. and Bout, R. G. (2004).
Scaling of jaw muscle size and maximal bite force in finches. J.
Exp. Biol. 207,2745
-2753.
Van der Meij, M. A. A., Griekspoor, M. and Bout, R. G. (2004). The effect of seed hardness on husking time in finches. Anim. Biol. 54,195 -205.
Verwaijen, D., Van Damme, R. and Herrel, A. (2002). Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lactertid lizards. Funct. Ecol. 16,842 -850.[CrossRef]
Wainwright, P. C. (1991). Ecomorphology: experimental functional anatomy for ecological problems. Am. Zool. 31,680 -693.
Warton, D. I. and Weber, N. C. (2002). Common slope tests for bivariate structural relationships. Biom. J. 44,161 -174.[CrossRef]
Willson, M. F. (1972). Seed size preference in finches. Wilson Bull. 84,449 -455.
Woltring, H. J. and Huiskes, R. (1990). Stereophotogrammetry. In Biomechanics of Human Movement (ed. N. Berme and A. Cappozzo), pp.108 -127. Wortington, OH: Bertec Corporation.
Ziswiler, V. (1965). Zur kenntnis des samenöffnens und der struktur des hörnernen gaumens bei körnerfressenden oscines. J. Ornithol. 106, 1-47.[CrossRef]
This article has been cited by other articles:
|
|
 |
|
  M. A. A. van der Meij and R. G. Bout The relationship between shape of the skull and bite force in finches J. Exp. Biol., May 15, 2008; 211(10): 1668 - 1680. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
