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Journal of Bionic Engineering 11 (2014) 282287

Frequency Analysis and Anti-Shock Mechanism of


Woodpeckers Head Structure
Zhaodan Zhu, Chengwei Wu, Wei Zhang
State Key Lab of Structural Analysis for Industrial Equipment, Dalian University of Technology, Dalian 116024, P. R. China

Abstract
The mechanical properties of the skull and the anti-shock characteristics of woodpeckers head were investigated by experiment and numerical simulation. We measured the micro-Youngs modulus of the skull by nano-indentation method and
calculated the macro-equivalent Youngs modulus of the skull at different positions using homogenization theory. Based on the
Computerized Tomography (CT) images of woodpecker head, we then built complete and symmetric finite element models of
woodpeckers skull and its internal structure and performed modal analysis and stress spectrum analysis. The numerical results
show that the application of pre-tension force to the hyoid bone can increase the natural frequency of woodpeckers head. The
first natural frequency under the pre-tension force of 25 N reaches 57 Hz, which is increased by 21.3% from the non-pre-tension
state and is more than twice the working frequency of woodpecker (20 Hz 25 Hz). On the application of impact force to the tip
of beak for 0.6 ms, high magnitudes of stress component occur at around 100 Hz and 8,000 Hz, far away from both the working
frequencies and the natural frequencies of woodpecker head. The large gaps among the natural, working and stress response
frequencies enable the woodpecker to effectively protect its brain from the resonance injury.
Keywords: woodpecker, anti-shock, frequency, modal analysis, stress spectrum
Copyright 2014, Jilin University. Published by Elsevier Limited and Science Press. All rights reserved.
doi: 10.1016/S1672-6529(14)60045-7

1 Introduction
Woodpeckers peck trees at a frequency of 20 Hz
25 Hz without causing cerebral concussion[1]. Their head,
which has the energy-absorption and anti-shock function,
has received much attention since 1979. Especially in
recent years, numerous experiments and numerical
simulations have been carried out to find out the
anti-shock mechanism of the woodpecker head.
May et al.[2] recorded the drilling action of an acorn
woodpecker using a high speed camera, and found that
the woodpeckers head moved in straight trajectory and
reached the maximum speed of 5 ms1 7 ms1 and the
deceleration of 600 g 1500 g within a 0.5 ms 1 ms
impacting duration. On the same impacting duration, the
human beings brain would be injured severely as the
upmost tolerance is only 300 g deceleration[3]. Gibson[4]
compared the skull structure and impact resistance of
woodpeckers with those of human beings. They proposed that small sized head, short impact duration and
large contact area between brain and skull will be beneCorresponding author: Wei Zhang
E-mail: wei.zhang@dlut.edu.cn

ficial for alleviating the injury to brain upon shock. Oda


et al.[5] set up a stereo lithography head model which is
three times larger than the actual head, and measured the
strain of the model under 2 N impact force experimentally. Then a 2D Finite Element (FE) model was built to
prove that little cerebral liquid and the existence of hyoid
bone can effectively protect its brain from shock damage.
In experiments, Zhou et al.[6] found the hyoid is composed of the fiber-typed hierarchical micro-structure,
which renders the hyoid high strength and good flexibility.
Yoon and Park[7] simplified the head structure as a
mass-damper-spring model and made the bio-inspired
shock-absorbing equipment consisting of close-packed
micro-glasses. The equipment can protect the micro
mechanical and electronic device in it from high-g
damage. Wang et al.[8] found that the pecking force and
velocity are around 8 N and 7.6 ms1, respectively.
Based on the micro-CT scanning, they set up a FE model
and analyzed the pecking impact on the rigid wall. They
concluded that most of pecking forces were transferred

Zhu et al.: Frequency Analysis and Anti-Shock Mechanism of Woodpeckers Head Structure

by the longer beak during the pecking. Zhu et al.[9] observed that the upper beak is longer than the lower
one and interpreted the mechanism of shock absorption
in terms of stress wave propagation. The structure of
skull facilitates the spreading of the stress wave and
the viscosity of biomaterials decreases the stress amplitude.
The papers published in the literature so far were
mainly focused on the stress and strain in the woodpecker head and little is known on the frequency response characteristics of the head under shock. Based on
the CT scanning technology, in this paper, the woodpecker head model with hyoid was established. Then its
anti-shock characteristic was studied from the aspects of
modal analysis and stress spectrum analysis with particular attention to the natural, working and stress spectrum frequencies of the head.

2 FE model and material property


2.1 FE model
Woodpeckers have small head, little amount of
cerebrospinal fluid, big eyeballs, hard beaks and long
flexible hyoid bone. The hyoid bone is four times the
length of the beak with one end fixing on the right nostril
and the other end binding the skull tightly and stretching
out from the mouth to reinforce the head[6,10]. The
woodpecker investigated here is a female grey-faced one
widely living in the Northern China.
The FE model was obtained by the following procedure. The woodpecker was put on a CT scanning device and the inner structure of head can be discerned
through the CT images of scattered points. Then Mimics
and ProE software were used to establish 3D geometric
configurations by integrating the scattered points.
Eventually, the FE model of the head was obtained and
analyzed using Abaqus software.
2.2 Mechanical property experiment
The woodpecker skull is a small and spheroid-like
structure, and the typical tension test cannot measure the
local property of the skull. In this paper, we measured
the mechanical properties of the bone in different positions of the skull by nano-indentation (Triboindenter,
Hysitron TI-950, Hysitron, USA). Nano-indentation
method was thought as the primary technique for
measuring the mechanical properties of materials on
micrometer and nanometer scales[11,12]. Bone samples

283

Specimen

2 mm
Skull

Fig. 1 Positions of the samples on woodpeckers skull (the grey


zone is the brain in the skull).

with the average size of 2.5 mm2.5 mm were cut from a


green woodpecker skull using a sharp operation blade.
The marrow of the specimens was washed away with
deionized water. The resultant specimens were subsequently ultrasonicated in deionized water bath for 5 min
and then air-dried. As shown in Fig. 1, thirteen specimens were obtained along the symmetric line of the skull
and fifteen specimens were cut from one side part of the
skull.
The total twenty-eight specimens obtained from
different positions were placed on a stainless steel platform and applied with a trapezoidal load function from
50 N to 1,250 N. The average value of Youngs
modulus of the whole skull bone is 6.4 GPa 2.4 GPa,
which is comparable with the average modulus of bovine and cervine bones, being about 22 GPa and 14 GPa
respectively[13,14]. The coefficient of variation of measured Youngs modulus of each specimen ranges from
16% to 40%. The Youngs modulus of woodpecker skull
has large standard deviation, presumably owing to the
huge differences in micro-structures of the bone in different positions around the skull, as shown in Fig. 2.
Apparently, there are various microstructures in
SEM (Scanning Electron Microscope, Quanta 200, FEI,
the Netherlands) images, as diverse as plate-like (a, g),
layered (e, f), rod-like (d, h, etc.) and porous (j, k, etc.)
structures, indicating the non-uniform macro mechanical
properties. It is really hard, actually almost impossible,
to build up such a multi-scale FE model and get the
accurate resolutions. In response to this, we used
macro-equivalent modulus instead of the local micro-Youngs modulus measured by nano-indentation to
set up a continuum model. In the following section, we
will describe how to obtain the macro-equivalent
modulus using homogenization method.

Journal of Bionic Engineering (2014) Vol.11 No.2

284

kinds of micro-cell model of trabecular bones and obtained near linear relationship between macro-equivalent Youngs modulus and the Volume Fraction Ratio
(VFR) of the bone. In the structure of woodpecker head,
there are several microstructures similar to Chens micro-cells. Thus, we adopt the Chens method to calculate
the macro-equivalent Youngs modulus.
Here we denote macro-equivalent Youngs
modulus as EM, VFR of bone as VB, measured local
modulus as EL. The relationship among them is approximated to be linear, as expressed in Eq. (1).

EM = EL VB .
Fig. 2 SEM images of microstructures of the bone around
woodpecker skull.

Youngs modulus (GPa)

10
8
6

10

4
2

Volume fraction ratio (%)

100

12

Volume fraction ratio


Measured Youngs modulus
Macro-equivalent modulus

0
a

g
f
Position

Fig. 3 Volume fraction ratio of bone, local measured modulus and


macro-equivalent modulus around the skull.

Fig. 4 3D complete model of woodpecker head and hyoid. Note


that the modulus of the skull and hyoid is non-uniform.

2.3 Homogenization of the bone


Homogenization theory is widely used to calculate
the property of spongy and compact bone in biomechanics because bones usually have many different periodic micro structures[1518]. Chen et al.[17] set up six

(1)

EL was obtained in former experiments of each specimen.


We counted the number of pixels of the pores and the
bone in the high resolution SEM images and calculated
the values of VB in positions of b, c, d, h, i, j and k, as
shown in Fig. 2. As the microstructures of skull at positions of a, e, f, and g are denser and ordered, we assumed
the VB to be one. In this way, we got the EM of skull.
Fig. 3 shows the EL, VB, and EM in different positions of
skull. It is interesting that the modulus changes periodically along the symmetric line of the skull; the
maximum modulus is four times larger than the minimum one.

3 Modal analysis
The modal frequency is mainly dependent on the
modulus and mass. It has been verified that the biological fluids and soft tissue in the pores of the bone do
not affect the bones modulus significantly [1921]. Thus
we built a continuum model without tissue fluids, and
then assigned the macro-equivalent modulus and the
total mass (bone plus tissue fluids) to the skull. The
hyoid has non-uniform modulus and the modulus at
given positions was assigned to the corresponding value
in accordance to Ref. [6]. The other parameters regarding material properties can be found in our previous
paper[9] and finally the complete model of woodpecker
head was set up, as shown in Fig. 4. The top of the skull
and the middle of the hyoid have the maximum modulus
in the individual part.
The natural frequency is highly dependent on the
material properties and boundary conditions. To simulate the actual conditions, we fixed the woodpecker head
at the bottom of neck. As documented, the woodpecker
geniohyoid muscle contracts a millisecond before

Zhu et al.: Frequency Analysis and Anti-Shock Mechanism of Woodpeckers Head Structure

natural frequency of the head. Take the first natural frequency as an example, when the applied pre-tension is
increased from 0 N to 25 N, the natural frequency increases from 47 Hz to 57 Hz, see the inset to Fig. 5,
an increment of 21.3%. The results imply that the
application of pre-tension in hyoid can significantly
raise the natural frequency of head to alleviate resonance.

25 N
20 N
15 N
10 N
5N
0N

100
90
80
70

58
56
54

60

52

4 Stress spectrum analysis

50
48
46

50
1st

2nd

3rd

4th

5th

6th
Mode

285

1st Natural frequency


0

15
20
25
5
10
Pre-tension force of hyoid (N)

7th

8th

9th

10th

Fig. 5 The first ten natural frequencies of the woodpecker head


under 0 N to 25 N pre-tension force on hyoid.

strike[68], and the contraction of muscle will produce a


pre-tension force on the hyoid. We wonder whether the
woodpecker would change the frequency response of
head by applying pre-tension force on the hyoid. To
examine the effect of pre-tension force on hyoid, we
applied different pre-tension forces to the model of the
hyoid. As the maximum tension strength and the
across-section area of the hyoid were reported to be
about 131 MPa and 0.2 mm2 respectively[6], we estimated the maximum pull force of the hyoid bone is
around 26 N. As such, in the model, we assumed the
upper limit of pre-tension force to be 25 N. With one end
of the hyoid fixed on the nostril, the other end was pulled
with a force of 0 N to 25 N. The first thirty modes of
woodpecker head were obtained. It is found that they are
the local vibration occurring within the brain due to its
low Youngs modulus. The whole vibration frequency of
woodpecker head must be higher than the local one.
Fig. 5 shows the first ten natural frequencies of woodpecker head.
Fig. 5 indicates that the first ten natural frequencies
of woodpecker head are in the range of 47 Hz 100 Hz.
These frequencies are more than twice the working
frequency (20 Hz 25 Hz) of the woodpecker. Apparently, such natural frequencies can protect the woodpecker head from resonance damage when pecking the
trees. To imitate the contract of hyoid bone of a woodpecker on pecking, we investigated the effect of the
application of pre-tension forces on the natural frequencies of woodpeckers head. As illustrated in Fig. 5,
the larger the pre-tension force of hyoid, the higher the

We then studied the stress response of woodpecker


head under dynamic impact and the effect of distributed
modulus on stress wave. Based on the homogenization
theory, we got the macro equivalent Youngs modulus
around the skull and built complete model of woodpecker head. In dynamic analysis, the materials were set
as viscoelastic. The mean viscosity of fluid phase within
bone is 0.086 Pas according to the former research[22]
and we assumed the viscosity of bone is proportional to
the water content, the less the water, the smaller the
viscosity. Bone with higher Youngs modulus usually
has less water. As a result, the viscosity changes of skull
should demonstrate the opposite trend with respect to the
Youngs modulus.
As the reaction force of the wood when woodpecker pecking is about 8 N, we applied an 8 N force on
the tip of woodpecker beak for an impact time of 0.6 ms
in computing model[8,9], and then removed the force and
kept the head free attenuation for several milliseconds.
To save computation time in explicit analysis, we simplified the complete FE model to a symmetrical model
which contains about 256,000 nodes and 1,192,000 tetrahedral elements and finally ran the programs on
Dawning Cluster Workstation with 48 computation
nodes 120 GB memory. After a computation period of
40 days, the FE results were obtained.
In order to study the frequency characteristics of
stress wave in brain, we set fifteen monitoring points in
brain (shown in Fig. 6) to record the change of the stress
at different positions. The maximum stress value is below 20 kPa which is consistent with the former
research[9]. We take the monitoring point S8 as an example to analyze the frequency spectrum of stress wave.
Fig. 7 plots the stress wave and frequency spectrum of
the monitoring point of S8. The analysis lasts for 20 ms
with 0.6 ms impact interval and about 19 ms free attenuation. From Fig. 7a, we can see that stress wave

Journal of Bionic Engineering (2014) Vol.11 No.2

286

tude stress component are beyond the natural frequencies of the woodpecker head, indicating the brain can be
protected from resonance damage effectively.

Brain

5 Conclusion

View (b)
(b)

(a)

Fig. 6 Monitoring points in brain: (a) Monitoring points on


symmetric surface of brain, named after O; (b) monitoring points
on section surface of brain, named after S.

Stress (kPa)

20

(a)

10
0

10
0.000

0.005

Magnitude

0.010
Time (s)

0.015

0.020

8000 Hz

(b)

100 Hz

4
2
0
101

102

103
104
Frequency (Hz)

105

Fig. 7 Stress wave and frequency spectrum of S8 monitoring


point in brain. (a) Stress wave of S8 in impact direction; (b) stress
spectrum in frequency domain after FFT.

decreases immediately after the pecking, the value of


stress falls near zero at about 10 ms and change marginally until the next pecking. It is for this reason that the
figure may be expanded and the stress wave in time
domain can be obtained, which is essential for the frequency spectrum analysis. Then we performed a Fast
Fourier Transform (FFT) to the stress wave and got the
stress in frequency domain.
Fig. 7b shows the stress frequency spectrum of
monitoring point S8. The vertical coordinate stands for
the magnitude of stress component at certain frequencies.
It can be seen, there are mainly two high magnitude
frequency bands of stress component, one is near 100 Hz,
the other is near 8,000 Hz, and the magnitude of the
latter is the maximum. At the rest frequencies, the magnitudes of stress component are low and most of them
are similar. This means the frequencies of high magni-

The woodpecker head has the unique ability to


protect its brain from impact damage. In this paper, we
studied the anti-shock mechanism of the woodpecker
head and got the conclusions as follows:
(a) There are several kinds of micro-structure in
woodpecker skull, and the Youngs modulus around the
skull is non-uniform but changes periodically. The
maximum Youngs modulus appears at the top of skull.
It is believed that the non-uniform distribution of Young
modulus in the skull hinders the stress propagation.
(b) The application of pre-tension force to hyoid
bone can increase the natural frequency of woodpecker
head. The first natural frequencies are between 47 Hz
57 Hz, more than twice the working frequency, i.e. 20
Hz 25 Hz, of the woodpecker head. The frequencies of
high stress component appear near 100 Hz and 8,000 Hz
respectively, far away from the working frequencies and
natural frequencies of the head. The large gaps among
the natural, working and stress response frequencies
enable the woodpecker to effectively protect its brain
from the resonance injury.
(c) The inhomogenous mechanical property and
special structure of the woodpeckers skull inspire one to
design light engineering structure which not only itself
shows a good shock-absorbing function, but also can
protect the instruments or the important elements inside
the structure, for example, light and high performance
helmets, spacecraft, etc. The special design of the
woodpeckers skull also inspires us to improve the
g-force tolerance of micromachined devices at high-g
and high-frequency mechanical excitations.

Acknowledgment
This work was supported by the National Natural
Science Foundation of China (11272080) and the Doctoral Education Foundation of China Education Ministry
(20110041110021).

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