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First published online October 7, 2008
Journal of Experimental Biology 211, 3333-3343 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.020941
Comparison of smooth and hairy attachment pads in insects: friction, adhesion and mechanisms for direction-dependence
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
* Author for correspondence (e-mail: wf222{at}cam.ac.uk)
Accepted 19 August 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: adhesion, biomechanics, direction-dependence, locomotion, tribology
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Fibrillar adhesive systems have recently attracted much
attention from the engineering and physical sciences because they are
considered to be promising models for novel, biomimetic adhesives
(Aksak et al., 2007;
Glassmaker et al., 2004;
Gorb et al., 2007;
Hui et al., 2004;
Jagota et al., 2007;
Kim and Sitti, 2006;
Lee et al., 2008;
Menon and Sitti, 2006;
Schubert et al., 2008). The
fibrillar design is thought to convey a number of specific advantages, such as
superior performance on rough substrates
(Persson and Gorb, 2003),
effortless detachment (Autumn and Hansen,
2006; Autumn et al.,
2006a; Autumn et al.,
2006b; Federle,
2006), self-cleaning properties
(Hansen and Autumn, 2005) and
increased adhesion due to contact splitting
(Arzt et al., 2003). However,
hairy and smooth adhesive pads have evolved repeatedly in different taxa
(Beutel and Gorb, 2001;
Gorb et al., 2002), and it
appears that both designs fulfil the requirements for successful climbing on
diverse substrates. Surprisingly, it is still unclear whether the performance
of the two designs is any different and, if so, in what respect. Smooth and
fibrillar adhesive systems have been the subject of recent reviews
(Autumn, 2007;
Barnes, 2007;
Federle, 2006;
Gorb, 2007;
Persson, 2007). However, no
previous study has explicitly compared the performance of these systems under
controlled conditions, and there exists a lack of information regarding the
forces that can be supported by these systems in insects. This study attempts
to address this by comparing a representative example of each, the hairy pads
of the leaf beetle Gastrophysa viridula De Geer (Coleoptera) and the
smooth arolium of the stick insect Carausius morosus Brunner
(Phasmatodea) (Fig. 1).
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;
Eisner and Aneshansley, 2000;
Federle et al., 2002;
Gorb, 1998;
Langer et al., 2004). This
mediates attachment through capillary and viscous forces and may help overcome
the problem of rough substrate attachment by filling in surface crevices. It
has been shown, however, that a build-up of fluid is detrimental to the
performance of smooth pads on smooth substrates due to the smaller forces
resulting from a thicker fluid layer
(Drechsler and Federle, 2006).
As such, in the present study, we tested whether a similar effect occurs in
the hairy system.
Insects with hairy and smooth pads can generate very high attachment forces
(Eisner and Aneshansley, 2000;
Federle et al., 2000). While
strong adhesion may be beneficial in many situations, it can make locomotion
more difficult. The problem of how to effect a controlled, energy-efficient
detachment is of particular importance to leaf-dwelling insects, which must be
capable of adhering to a range of demanding substrates while still being able
to rapidly detach (for example during the pursuit or evasion of other
animals). A fundamental property of adhesive structures that helps to achieve
rapid and controllable adhesion during locomotion is their
direction-dependence. It has been observed that friction and adhesion forces
of most animal attachment organs are higher when pulled towards the body (i.e.
proximally) rather than pushed away from it (i.e. distally). Previous studies
have shown this to be the case in hairy adhesives of geckos, spiders and flies
(Autumn et al., 2000;
Autumn et al., 2006a;
Hill, 1977;
Niederegger and Gorb, 2003) as
well as in smooth adhesive pads of ants, bushcrickets and cockroaches
(Clemente and Federle, 2008;
Federle et al., 2001;
Federle and Endlein, 2004;
Gorb and Scherge, 2000).
However, the detailed mechanisms underlying direction-dependence are still
not sufficiently understood in either smooth or fibrillar systems. It is
unclear whether direction-dependence is achieved through changes in contact
area or through a change in shear stress (i.e. friction force per unit contact
area). Analysing the smooth euplantulae of the bushcricket Tettigonia
viridissima, Gorb and Scherge proposed that friction is
direction-dependent due to the bending and reorientation of the inner rods of
the pad cuticle (Gorb and Scherge,
2000). However, this hypothesis does not specify whether the
action of the rods during a proximal pull is thought to increase pad contact
area or shear stress. Large direction-dependent changes of contact area can
occur in adhesive pads that can be unfolded. It has been shown for ants and
bees that changes of adhesive contact area are mediated both by the action of
the claw flexor muscle and by the passive unfolding of the pad when legs are
pulled towards the body (Federle and
Endlein, 2004; Federle et al.,
2001). However, even in the absence of such an unfolding
mechanism, direction-dependent changes of contact area can be brought about by
the flexibility of the chain-like tarsus. This has been shown for the
cockroach Nauphoeta cineraea, where a distal movement of the
unrestrained tarsus caused a peeling detachment of the smooth arolium
(Clemente and Federle,
2008).
For the fibrillar adhesive system, previous explanations of
direction-dependence have focused on the behaviour of individual setae.
Adhesive hairs of geckos are non-symmetrical and feature distally pointing
setae and spatulae, which have been shown to generate higher friction and
adhesion when aligned with a proximal pull
(Autumn and Hansen, 2006;
Autumn et al., 2000;
Autumn et al., 2006a;
Gravish et al., 2008). Without
a proximal pull, only the ends of the spatulae will contact the surface,
representing only a small fraction of the total possible contact area. This
results in a highly direction-dependent friction on the level of individual
hairs. However, fibrillar adhesive systems have a hierarchical structure, and
attachment and detachment may not only be controlled on the level of
individual setae/spatulae but also on the level of setal arrays (pads) and the
foot (tarsus) as a whole. It is still unclear what contribution each of these
levels makes to directional dependence and to attachment and detachment during
locomotion.
The fibrillar systems of beetles are similar to those of geckos in many
aspects. Although several other hair types exist, spatula-tipped setae
represent the prevalent design (Stork,
1980) and may well exhibit similar properties to gecko setae.
Tarsal movements involved in attachment and detachment have been recorded in
flies (Niederegger and Gorb,
2003). However, no observations have been made on the dynamic
changes of adhesive contact area in any fibrillar system and the presence of a
directional-dependence has yet to be confirmed for insects with hairy adhesive
pads.
The aim of this study was therefore to compare the performance of smooth and fibrillar systems in insects and to clarify their mechanisms of direction-dependence. By measuring frictional and adhesive forces in two model organisms, the leaf beetle G. viridula and the stick insect C. morosus, we address the following questions: (1) how do smooth and hairy systems compare in terms of their adhesive and frictional performance, (2) how does the fluid pad secretion influence attachment in fibrillar systems, (3) are forces in smooth and hairy pads direction-dependent and (4) what is the mechanism for this direction-dependence, if present?
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Vincent and Wegst,
2004), the functional properties of insect adhesive pads can only
be investigated in vivo. As such, live adult stick insects, C.
morosus, and male dock beetles, G. viridula, were taken from
laboratory colonies, weighed and mounted on glass cylinders. Stick insects
(body mass 898±31 mg, mean ± s.e.m.) were enclosed inside the
glass cylinder so that a single leg protruded. We isolated the leg using
PlasticineTM and secured it to a firm piece of wire (attached to the
glass cylinder) using dental cement (ESPE Protemp II, 3M, St. Paul, MN, USA).
The claw tips were clipped with micro-scissors to prevent them from
obstructing the arolium. Beetles (body mass 10.4±0.4 mg, mean ±
s.e.m.) were immobilised by enclosing them in Blu Tack and Parafilm tape, with
the Blu Tack used to isolate the leg. Front and rear legs were used. The tarsus of C. morosus has five segments, the first four of which bear euplantulae on the ventral side. The leg terminates with a pretarsus that bears the claws and the smooth adhesive arolium (see Fig. 1D–F). The tarsus of G. viridula consists of five segments and a distal pretarsus bearing the claws. The fourth segment is reduced and sunken into the larger third tarsomere. The ventral sides of the first three tarsomeres are densely covered by adhesive setae. Setae are typically curved and oriented distally and belong to three principal types: (a) pointed, with a tapered end, (b) flat, spatula-tipped and (c) disk-tipped, with a marginal bulge. Due to sex-specific variation in the abundance of the different types of setae, only male beetles were used in this study. The distal-most pad on the third tarsomere (Fig. 1A–C) was used throughout this study for force measurements.
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General setup
Following a previous study (Drechsler
and Federle, 2006), a force transducer setup was used to measure
friction forces of the pad while simultaneously recording contact area
(Fig. 3). Forces were measured
with a self-built, two-dimensional force transducer employing 350
foil
strain gauges (1-LY13-3/350, Vishay, Malvern, PA, USA) and fixed to a
three-dimensional DC motor stage (M-126PD, Physik Instrumente, Karlsruhe,
Germany). The force transducer was calibrated with calibration weights and by
applying defined displacements to obtain the spring constant at different
lever arm lengths. The stage was controlled with custom-made LabVIEW (National
Instruments, Austin, TX, USA) software that allowed a precise set of
user-defined movement patterns. Voltage output was amplified
(ME-Meßsysteme, Henningsdorf, Germany) and sampled at 1000 Hz with an
I/O board (PCI-6035E, National Instruments). The LabVIEW programme included a
normal force feedback mechanism that allowed friction experiments to be
performed while keeping the normal force constant. The force feedback
mechanism consists of a 50Hz feedback loop, in which the programme computes
the deviation between a set-point force and the actual force and passes this
on to a discrete PID control algorithm to compute a displacement, which would
compensate the error. The distal-most footpad was brought into contact with a
glass plate (18 mmx18 mmx0.1 mm) attached to the strain-gauge
transducer. Contact area was visualised using a coaxially illuminated
stereomicroscope, which shows actual contact as a high-contrast silhouette
(Federle et al., 2002). Images
were recorded using either a Redlake PCI 1000 B/W camera (for smooth pads)
(Tallahassee, FL, USA) or a high-speed digital HotShot PCI 1280 B/W camera
(NAC image technology, Simi Valley, CA, USA) (allowing the higher resolution
necessary to image hairy pads) and were analysed with MATLAB (The Mathworks,
Natick, MA, USA) scripts. For the hairy pads, a `projected' pad area was also
measured by manually plotting a solid polygon around the outermost setae in
contact to allow the basic frictional force per total pad area to be compared
between hairy and smooth systems.
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Experiments to measure attachment performance
For both animals, proximal friction slides (corresponding to a pull of the
leg towards the body) were performed at 500 µ ms–1 over 10
mm. The relatively large sliding distance was chosen to ensure that the pads
were sliding at the same velocities and to be able to test the effects of
fluid accumulation and depletion. Distal friction slides (corresponding to a
push of the leg away from the body) were done in the same way but were
preceded by a short, 0.5 mm proximal slide. This was done because previous
studies (Autumn et al., 2000;
Gravish et al., 2008) and
preliminary observations had suggested that a proximal movement following
contact was beneficial in aligning the footpads and ensuring proper contact.
For the beetles, the normal force feedback kept the load constant at 0.1 mN
during the slide, corresponding to 98% of the body weight of the beetle and to
a load stress (force per projected contact area) of 1.7 kPa. This was raised
to 1 mN for the stick insects (corresponding to 11% of the body weight and a
load stress of 9.8 kPa) to achieve a compromise between a comparable fraction
of the insect's body weight and a comparable load stress. Our results show
that this difference of normal forces and load stresses has a negligible
effect on friction and shear stresses (see below). Otherwise, conditions were
kept identical for both insects during all slides. For the footloose
condition, no feedback was used during the slide because otherwise the
flexibility of the tarsal chain caused the leg to bend and bring other pads
into contact. Adhesion area was not recorded for the distal slides as, in most
cases, the visible contact area at the end of the slide had dropped below a
range that could produce meaningful, noise-resistant results. Similarly,
projected area was not calculated for distal slides as the pad outline was
often small and irregular.
To investigate the function of the pad secretion in the hairy system (and
to control for its effects), repeated proximal slides were performed as above
for the immobilised dock beetle. Nine consecutive slides (separated by a 3 s
pause following each pull-off) were carried out either on the same area of the
glass plate (intended to allow the fluid to build up) or on a fresh area
(intended to allow the fluid to deplete). The fluid accumulation on the glass
substrate was visualised using Interference Reflexion Microscopy (
=546
nm, x20 magnification, Leica DRM, Wetzlar, Germany). Consecutive slides
were statistically analysed using Page's non-parametric L test
(Page, 1963), where the
indices Lm,n indicate the number of conditions
(m) and the sample size (n).
Due to the considerable influence of the amount of secretion on friction forces, all `immobilised' slide movements were repeated following two regimes: (1) `little secretion' – each slide was performed on a clean area of glass plate and (2) `accumulated secretion' – four consecutive, proximal slides were performed first on the same area of the glass plate to allow the pad secretion to build up. We recorded forces in both conditions in order to reduce variation caused by variable amounts of secretion present in the contact zone. At the end of every slide, a 5 s pause was left to allow friction to drop before performing a 500 µms–1 perpendicular pull-off. This allowed adhesion forces to be measured.
To test the effect of applied normal force on sliding friction and shear
stress, we measured forces for G. viridula and compared this with
already published, analogous measurements for stick insects
(Drechsler and Federle, 2006).
Proximal and distal slides (little secretion) were performed as above but with
the applied normal force varied at 0.1, 1.0 and 5.0 mN.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Effect of fluid secretion on friction and adhesion in the hairy system
To evaluate the effect of the amount of adhesive secretion in the hairy
system, we measured friction and adhesion during proximal slides under two
different regimes in Gastrophysa. When slides were repeated on the
same area of glass (fluid build up), friction and adhesion strongly decreased
from slide to slide until they approached a plateau (mean shear stress
decreasing to 42% from slide one to nine; adhesive stress decreasing to 52%).
As contact area remained largely unchanged, this effect was due to a highly
significant decrease of both adhesive stress (adhesion per unit area) and
shear stress (friction per unit area) (Page's L test, adhesive
stress, L9,5=1310, P<0.001; shear stress,
L10,5=1888, P<0.001)
(Fig. 5A,C). On the contrary,
repeated slides, each time on a fresh area of glass (fluid depletion), showed
no significant drop and in fact showed a significant upwards trend in shear
stress (Page's L test, adhesive stress,
L9,5=1138, P=0.396; shear stress,
L10,5=1665, P=0.007)
(Fig. 5B,D). The increase in
shear stress mainly occurred from the first to the third slide (Page's
L test from first to third slide, L3,5=68,
P=0.0089), and subsequent forces remained constant, producing highly
reproducible curves between consecutive slides (Page's L test from
third to tenth slide, L8,5=816, P=0.44). This
indicates that the amount of fluid in the contact zone was depleted over the
first three slides and reached a constant level after that. An example image
of the build up of pad secretion is presented in
Fig. 6. It can be seen that
there are many more fluid droplets deposited on the glass surface in the
`accumulated' condition. These droplets represent the persistent, hydrophobic
component of adhesive secretion (Federle
et al., 2002). Fluid build up and fluid depletion have a similar
effect in C. morosus (see Table
1) (Drechsler and Federle,
2006), and the results presented in the current study demonstrate
that this is equally present and conspicuous in the fibrillar pads of
Gastrophysa.
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Effect of applied normal forces on friction, contact area and shear stress
The effect of normal force was investigated in G. viridula by
performing proximal slides at three different applied forces (0.1, 1.0 and 5.0
mN). Despite a 50-fold variation of load, we did not observe any significant
change in friction, contact area or shear stress
(Fig. 7). The lack of an
increase in contact area with load differs markedly from our previous findings
for stick insects (Drechsler and Federle,
2006) (see Table
1). This finding is consistent with the morphology of both types
of attachment pad (Fig. 1). The
seta tips in G. viridula are almost coplanar so that, even at very
small normal forces, all setae make contact if the pad is properly aligned
with the substrate. By contrast, the arolium of C. morosus is
hemispherical, resulting in an increase of contact area with load as predicted
by the JKR theory (Johnson et al.,
1971). However, in both G. viridula and C.
morosus, shear stress was independent of load, confirming that friction
forces are fully determined by contact area in both systems
(Table 1). As a consequence,
the comparison of shear stress between the smooth and hairy adhesive systems
in this study is not affected by changes to normal force.
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Direction-dependence in smooth and hairy pads: level of adhesive pad
We quantified the effect of sliding direction in smooth and hairy systems
by performing proximal and distal slides in a randomised order. We evaluated
both the maximum friction during the slide and the adhesion force peak during
the pull-off at the end of each slide. As friction forces of beetles and stick
insects were strongly dependent on the amount of fluid present in the contact
zone [Carausius (Drechsler and
Federle, 2006); Gastrophysa, see above], slides were
performed in both the `little' secretion and the `accumulated' secretion
regimes (see Fig. 8). In both
animals and both conditions, maximum friction was significantly lower in the
distal direction (Table 2;
Fig. 8). However, frictional
forces decreased more strongly in the hairy system (mean little secretion,
7.8-fold in G. viridula vs 2.3-fold in C. morosus; mean
accumulated secretion, 3.4-fold in G. viridula vs 2.7-fold in C.
morosus).
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Contact area was measured simultaneously, allowing friction forces to be
normalised for area (see Table
2). In both systems, contact area visibly decreased during distal
pushes (most differences were significant;
Table 2). The contact area of
the hairy system showed conspicuous changes during the slides. During proximal
slides, adhesive contact area was maximal and any hair tips not already in
contact after the initial preload were brought into full contact at the start
of the slide. However, during distal slides, hair tips appeared to peel off
individually and decreased in contact area
(Fig. 9). This resulted in the
distal slides taking place with only what appeared to be the setal tips in
contact. The tips appeared to remain in contact with the surface, the hairs
bending or tilting to allow this. The deflection of setae was manifested
visually by a movement of the contact zones relative to the pad. This
displacement was measured by comparing the positions of the distal end of the
contact zone during the short proximal and subsequent distal slides (measured
at the force peaks) using a MATLAB script. Excluding three slides where the
movement of the distal edge was difficult to track reliably, the hair contacts
moved by 68.1±4.4 µm in the proximal–distal direction (little
secretion, mean ± s.e.m.). This is greater than the length of the setae
(40–50 µm) (Orso et al.,
2006) and corresponds to a large bending or rotation of the hairs
from being distally to being proximally angled.
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Shear stress was computed using real observed contact area. For stick insects, shear stress showed no significant change between proximal and distal slides (Table 2; Fig. 8). This shows that the higher friction forces in the proximal direction are not explained by shear stress but by an increase in contact area. However, for the beetles, shear stresses were higher in the proximal direction (significant difference in the little secretion regime; see Table 2). Thus, the frictional direction dependence in Gastrophysa is not only based on a higher contact area but also on an increased shear stress during proximal slides.
Similar to the friction forces, adhesion was much smaller after a distal slide in both smooth and hairy systems (differences were highly significant; Table 2). This clearly confirms that adhesion is strongly influenced by shear forces towards or away from the body, thus providing a way of controlling attachment and detachment.
It should be noted that despite the 3 s stop of the motor movement at the end of each slide, there was still a significant shear force present during the pull-off movement. Thus, the effective force vector was not perpendicular to the surface but the mean detachment angles were: C. morosus 20.61±2.64 deg. proximal, 168.44±3.91 deg. distal; G. viridula 32.36±2.76 deg. proximal, 114.52±4.80 deg. distal (all presented for little secretion).
For both animals, the frictional force generated by a single pad in the proximal direction was more than sufficient to support the body mass of the animal. However, this was not the case for the distal adhesion of C. morosus (mean body weight, C. morosus, 8.81±0.30 mN; G. viridula, 0.102±0.004 mN).
Direction-dependence in smooth and hairy pads: level of whole tarsus
Footloose slides (where the tarsal chain was left free to move) were
performed both proximally and distally. This was done in order to investigate
whether and how the flexible tarsus contributes to the observed
direction-dependence of friction forces. Slides were performed in the same way
as for the immobilised condition, with the exception that the feedback had to
be left out to prevent the proximal tarsus or the tibia from touching the
substrate. We therefore performed footloose trials with a constant
z-position of the motor after an initial force feedback preload.
During a proximal pull, good contact was made and was maintained throughout
the slide in both systems (Fig.
10A,C). However, during a distal push, tarsal instabilities were
apparent. For C. morosus, a distal push caused the tarsus to buckle
upwards, thereby peeling off the arolium from the proximal side and detaching
it rapidly from the surface (Fig.
10B). For G. viridula, the lateral flexibility of the
tarsal chain caused the leg to bend, mainly laterally, rotating the foot by
almost 180 deg. and preventing it from detaching
(Fig. 10D). However, this
behaviour is never observed in freely walking beetles and may be an artefact
resulting from the relaxed claw flexor muscle and the fixed tibia. As such,
additional observations were made where the beetle was mounted in Blu Tack as
for the immobilised condition but with greater freedom in the
dorsal–ventral direction. In this condition, a proximal slide showed
good contact, as before (Fig.
10E, as imaged from above, given that the side view was obstructed
with Blu Tack), whereas a distal push caused the entire pad to peel off from
the proximal to the distal side (Fig.
10F). As for C. morosus, this prevented any recording of
friction forces in the distal direction. Adjacent setae peeled and detached
together and we observed the propagation of `peeling fronts' across the pad
contact zone as a whole. However, this propagation was very fast and peeling
of individual setae occurred almost simultaneously over large contiguous areas
of the pad contact zone. This detachment of the whole pad was apparently
caused by a rotation of the tarsal segment within the sagittal plane due to
the torque introduced by the distal push.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
However, the opposite effect was found on a rough substrate, suggesting that
the fluid mainly serves to maximise contact on rough substrates. We believe
that this conclusion is also likely to hold for hairy pads of insects, where
the contact of relatively large seta tips is supplemented by a fluid
secretion. To compare adhesive and frictional performance between G. viridula and C. morosus, the most direct contrast is of the shear and adhesive stresses supported by each adhesive. Table 3 shows that stresses were slightly higher in G. viridula when calculated from spatula contact area, suggesting that the hairy system may represent a more efficient attachment mechanism. However, it is biologically more relevant to compare forces per projected pad area because this is the area available to the animal for generating adhesion and friction. Shear and adhesive stresses calculated from projected pad area, for the hairy system, were in most cases no longer significantly different and even slightly lower.
It has been proposed that the adhesive stress of fibrillar adhesives
increases as the dimensions of the individual contact elements decrease
(Arzt et al., 2003). This
`force-scaling' idea is based on the assumption that the adhesion of an
individual subcontact scales linearly with its radius of curvature (for
spherical contacts) or its width (for tape-like spatulae). The model further
assumes that the total adhesion of an array of setae is the product of the
force of a single seta and the number of setae. Thus, if the adhesive force of
a single subcontact scales with its width, w, and the number of
contact elements per pad area with 1/w2, then adhesive
stress, F/A, should increase when the subcontacts are made
smaller:
 | (1) |
This concept has been used to explain differences in contact size and
density across a range of animals with different body sizes because larger
animals with relatively less available surface area (such as geckos) are
expected to require a more effective adhesive system per unit pad area than
smaller animals [such as insects (Arzt et
al., 2003; Spolenak et al.,
2004)]. The fact that fibrillar adhesive pads of lizards are
characterised by a much higher contact density than those of beetles has been
seen as a confirmation of the `force-scaling' hypothesis
(Arzt et al., 2003). However,
Eqn 1 predicts the adhesive
stress of G. viridula (spatula width approximately 6 µm) to be
30x smaller than that of a Tokay gecko [Gekko gecko, spatula
width approximately 0.2 µm (Williams
and Peterson, 1982)]. The mean adhesive stress of arrays of gecko
setae has been measured as 53±7.6 kPa
(Gravish et al., 2008), which
is only slightly higher than our values for G. viridula and C.
morosus. As the adhesive stress values compared in the present study were
measured under different conditions, any conclusions have to be treated with
caution. The comparison is also being made between different species and
adhesive systems (wet vs dry) and this is an important caveat.
However, despite this, these values certainly suggest that gecko pads do not
in fact have a much higher efficiency per unit attachment area, in contrast to
the prediction from Eqn 1. This
conclusion is consistent with recent data on the scaling of adhesive hair
dimensions across different taxa (Peattie
and Full, 2007), which suggest that differences in seta density
are mainly explained by phylogenetic background and the presence or absence of
an adhesive fluid (as is the case here for the dry gecko and the wet insect
system) rather than by force scaling. Eqn
1 is also inconsistent with the almost identical adhesive stress
in a smooth (C. morosus) and a hairy system (G. viridula),
as found in the present study.
A possible explanation is that the assumptions of the force-scaling model
do not hold for animal adhesive pads. First, load may not be `shared' equally
by all the setae of an array. If hairy pads detach from a surface by peeling
(as observed during the footloose experiments), stress is concentrated at the
edge of the pad so that only a small number of setae contribute to the total
force (Hui et al., 2004). In
this case, pad pull-off forces would not be correctly predicted by the
force-scaling model. Second, the adhesive forces of individual subcontacts
might not scale with their width or radius but might scale with contact area,
removing any scaling advantage from seta miniaturisation
(Gao and Yao, 2004;
Spolenak et al., 2004). This
could be achieved, for example, through spatulae that have an optimised
concave shape, giving rise to a uniform stress distribution in the adhesive
contact zone at pull-off (Gao and Yao,
2004; Spolenak et al.,
2004). In fact, adhesive setae in several insects (including
G. viridula) are known to have concave spatulae
(Haas and Gorb, 2004;
Langer et al., 2004).
If the efficiency of gecko and beetle pads is indeed of a similar
magnitude, it is unclear how geckos compensate the size-related loss of
mass-specific adhesion. Assuming isometry, the surface-to-volume ratio of
G. gecko can be estimated to be approximately 16x smaller than
that of G. viridula [body masses, 10.4 mg vs 43.4 g
(Irschick et al., 1996)].
Geckos may partly compensate for this through disproportionately larger
adhesive pads [estimated total pad areas, 0.47 mm2 vs
227.1 mm2 (Irschick et al.,
1996)]. However, given that the pull-off forces of G.
viridula are extreme, with the force of a single pad on a smooth surface
corresponding to more than 10x the body weight of the beetle
(Table 2), geckos may simply
have a smaller `safety factor' and still adhere perfectly well.
The above arguments apply only to smooth substrates. Most biologically
relevant substrates, however, possess some degree of surface roughness. Theory
predicts that fibrillar systems, and in particular arrays of branched setae
with fine endings as found in geckos, should make better contact to rough
substrates (Persson, 2003;
Persson and Gorb, 2003).
However, it still remains to be investigated experimentally whether the
performance on rough substrates differs between smooth and wet or dry
fibrillar pads.
Mechanisms for direction-dependence
In order to consolidate fast running with effective attachment, an adhesive
system must allow rapid and energy-efficient detachments. Both smooth and
hairy adhesive pads of insects possess this ability. The direction-dependence
of adhesive and frictional forces is probably a key adaptation for the dynamic
control of surface attachment. Our findings demonstrate that smooth and hairy
systems both showed this anisotropy when comparing proximal (a pull of the leg
towards the body) and distal (a push of the leg from the body) slides. Distal
friction forces were always much lower in both little and accumulated
secretion regimes and showed a significant decrease in contact area. Adhesion
forces were also greatly reduced following a distal slide and, for the
conditions used, demonstrate an increased ease of detachment.
|
). However, in the hairy system of the beetles,
the higher friction in the proximal direction was not only due to a strongly
increased area of contact but also due to a higher shear stress. This suggests
that the `quality' of the adhesive contact differed between proximal and
distal sliding.
Fig. 9 shows that the
changes in contact area occurred at the level of each individual hair. During
the proximal pull (Fig. 9A),
all hairs made good contact with the surface, and a high resultant force was
observed. However, during the start of a distal push
(Fig. 9B–E), the spatulae
of each hair began to lose contact. They appeared to peel from the surface and
remain with this small fraction of contact during the slide. The hairs are
typically angled in the distal direction
(Beutel and Gorb, 2001) and,
as such, the resulting steeper peel angle may aid detachment during a distal
push, allowing individual hairs to peel from the proximal side. By contrast, a
proximal pull would put the hairs into tension, the shallow angle acting
against contact peeling (Autumn et al.,
2006a; Federle,
2006) (see Fig.
11). For immobilised pads, the fibrillar design had a more
pronounced direction-dependence, with a 7.8-fold drop in friction, a
considerable decrease compared with the 2.3-fold drop for the smooth system
(little secretion). Unlike the smooth system, which can detach at just one
peel edge, the hairy system in beetles has several hundred contacts that can
peel independently and almost simultaneously, which may aid rapid
detachment.
The observed decrease in shear stress may be partly a result of overestimating the area of the seta tips that is in close contact. This could arise from fluid-filled, near-contact being observed in the coaxial illumination and being included in the contact area calculation (see Fig. 11). This idea gains support when taking into account the calculated change in contact area for both secretion regimes. The change for accumulated secretion was considerably less than the corresponding drop for little secretion (a 1.5x decrease compared with a 3.7x decrease), implying that the increased presence of fluid may well contribute to the measured area.
The footloose slides of the stick insect showed that the tarsus itself
contributes to a loss of contact area in the distal direction through
buckling. Instabilities in the tarsal chain rapidly increase the angle between
the leg and the surface, allowing the pad to peel from the proximal side. This
adds to previous observations of the same effect in cockroaches
(Clemente and Federle, 2008)
and implies that, due to its construction, the tarsus, and to some degree the
pad itself, is unstable when pushing. The foot as a whole also contributed to
pad detachment in the beetles, adding to the direction-dependence of
individual setae. This was less clearly demonstrated by the original footloose
experiments but further observations made with a semi-restrained tarsus showed
a similar proximal–distal peeling detachment as observed for the
footloose stick insects.
Our results show that adhesion strongly depends on the sliding direction
before pull-off. When pull-off and proximal/distal shear forces act
simultaneously, the effect is very similar. Recent work on geckos has shown
the presence of a critical detachment angle at the level of single setae,
arrays of setae and the whole toe (Autumn
and Peattie, 2002; Autumn et
al., 2006a; Gravish et al.,
2008). Detachment occurs as soon as the angle of the force vector
exceeds the critical angle. As some proximal shear is required for the setae
to adhere, this effect has been termed `frictional adhesion'
(Autumn et al., 2006a).
Direction-dependence of adhesive structures is the precondition for
controlling attachment and detachment via the amount of proximal or
distal shear force. The present results suggest that both C. morosus
and G. viridula might control adhesion in a similar way as the gecko.
However, further work is needed to determine the detailed angle dependence of
adhesion in both systems.
The directional behaviour of the hair tips represents a specialised passive
mechanism to control adhesion. Biomimetic directional adhesives have many
possible applications and first prototypes have already been fabricated
(Autumn et al., 2006a;
Lee et al., 2008;
Schubert et al., 2008).
However, before design principles can be effectively transferred into
technical applications, a greater understanding is needed of their precise
function in the natural systems. Our study illustrates that there is still
much to investigate about both smooth and fibrillar adhesive systems in
animals.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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