Adhesion measurements on the attachment devices of the jumping spider Evarcha arcuata
Department of Zoology, Technical Biology and Bionics, Saarland University, D-66041 Saarbrücken, Germany
* Author for correspondence (e-mail: a.kesel{at}rz.uni-sb.de)
Accepted 6 May 2003
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Summary |
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Key words: dry adhesion, ultrastructure, scopula, claw tuft, seta, setule, safety factor, atomic force microscopy, scanning electron microscopy, spider, Evarcha arcuata
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Introduction |
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An analogous ultrastructure is found in spiders. In addition to the tarsal
claws, which are present on the tarsus of all spiders, adhesive hairs can be
distinguished in many species. These adhesive hairs are either distributed
over the entire tarsus, as for example in Lycosid spiders
(Rovner, 1978), or
concentrated on the pretarsus as a tuft (scopula) lying ventral to the claws
(Hill, 1977
), as also found in
the jumping spider Evarcha arcuata (Salticidae), where a scopula is
found on each pretarsus. So far, the effectiveness of these attachment
structures has not been analysed. In the present study, the adhesive force
(Fa) of the cuticular scopula was analysed via
atomic force microscopy. This method permits highly localised measurements of
mechanical surface parameters (Binning et al., 1986;
Radmacher et al., 1994
) and,
thus, for the first time, the determination of the adhesive characteristics of
the tiny terminal ends (setules) that supply the initial contact area with the
substrate (Fig. 1).
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Materials and methods |
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Scanning electron microscopy
Prior to SEM studies, individuals were dehydrated in ascending acetone
concentrations (70%, 80%, 90%, 100%), cleaned with ultrasound,
critical-point-dried (CPD 030 Critical Point Dryer; Bal-Tec, Witten/Ruhr,
Germany) and sputter-coated with gold (SCD 005 Sputter Coater; Bal-Tec).
Specimens were examined in high vacuum using a Zeiss DSM 940A electron
microscope at 1015 kV.
Atomic force microscopy
In order to carry out adhesion measurements with AFM, untreated individuals
captured shortly before use were supinely embedded in 5-min epoxide resin
(R&G GmbH, Waldenbuch, Germany). Scopula hairs were kept free of the
embedding medium. To ensure that the mechanical properties of the setules were
not altered by a covering layer of epoxide, capillary rise of the fluid resin
between the setules was avoided by a short waiting period prior to embedding
of specimens (resin curing time approximately 1.5 min). Further preparations
were not necessary for this measuring technique. Measurements were
accomplished under ambient conditions (23°C; 45% air humidity).
A commercial AFM (Topometrix® Explorer; controller software
SPMLab 4.01; Santa Clara, CA, USA) was used to measure the adhesive force of
the terminal setule contact area. Pointspectroscopy was performed in order to
obtain data. In doing so, a highly local contact between certain defined
points on the sample and the instrument's probe was established. According to
Hartmann (1991), this
application of ATM is especially suitable for determining van der Waals forces
of samples. In this case, the probe was an ultrathin siliconnitride
cone, mounted on a cantilever. Prior to the actual probing of the setule
surface, the cantilever was lowered towards a glass surface and tapped onto
the latter. Due to this dynamic contact, the cone-shaped probe tip was
flattened, which allowed us to assume a two-dimensional, flat contact area for
the probe tip when interacting with the setules. Probe tip area
(3.6x105 nm2) was determined using SEM, as was the
successful flattening of the probe tip. The cantilever had a spring constant
of 5.95 N m-1. At a constant velocity (0.5 m s-1), the
probe was slowly brought into contact with the sample and then retracted,
passing through a predetermined traverse path (l; 200400 nm;
maximum error, ±4 nm). Contact was made perpendicular to the ventral
surface of the scopula. The traverse path l was registered by a
linearised scanner (EX 179807) via strain gauge. Due to the probe's
low driving velocity, load application was taken as quasi-static
(Burnham and Kulik, 1999
).
During probesample contact, the cantilever was deflected, in turn
leading to the deflection of a laser beam that was projected on the upper
surface of the cantilever. Laser deflection was measured by the change in
current of a photodetector. This change in current served as a measurement
signal directly related to the traverse path and was recorded by an internal
data processor. The current changes were converted to force values based on a
previous calibration of the instrument. The calibration of the experimental
set-up was accomplished by applying known masses to the cantilever and
recording the occurring current alterations. A calculated regression equation
obtained in this process served as a calibration curve. The internal AFM
measurement error for the registered forces accounted for a maximum of 10%. No
further data processing was performed. Data were plotted as a
forcedistance curve in which the readings of the `pull-off' forces
during spontaneous detachment of probe and sample represented the adhesive
force Fa between the two
(Fig. 4;
Radmacher et al., 1994).
Control measurements were conducted on glass as well as with the epoxide used
(resin curing time approximately 1 h under ambient conditions).
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Results |
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With a mean setule density of 2.1±1.0 setules µm-2 (N=48) or 2.1x106 setules mm-2 on the setae's ventral side and an estimated scopula area of 0.037±0.008 mm2 (N=4) per scopula, a single foot is provided with roughly 78 000 setules. This gives a total of more than 624 000 possible contact points with a substratum for all eight feet.
Atomic force microscopy
Using the recorded data from pointspectroscopy
(Table 1), as well as estimates
of areas obtained from the SEM micrographs, the total force of adhesion,
Fa, was calculated as follows.
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The contact area of the probe tip (3.6x105 nm2) was clearly larger than the surface area of the setule tips (1.7x105 nm2; see Fig. 3). Thus, the possibility arises that the probe tip comes into contact with more than one setule at a time. Such multiple events are easily identified by their `stepped' pull-off character, and curves that contained such multiple pull-off events were not taken into consideration for the further calculation of adhesive forces. Therefore, we assume that the terminal setule tip represents the relevant adhesive contact area. A mean Fa of 38.12±14.6 nN (N=45; Fig. 4) was obtained from the forcedistance curves of the AFM measurements. Thus, the mean adhesion was 38.12 nN per setule.
Given an estimated 78 000 setules or contact points per scopula, a single
foot is calculated to produce an adhesive force of 2.97x10-3
N when contact to the substrate is maximal. Providing that all eight feet or,
respectively, all eight scopulae are in full contact with the underlying
surface, adhesion perpendicular to the substrate would measure
2.38x10-2 N, and the tenacity [n; the ratio
of Fa to contact area (A)] would then be
2.24x105 N m-2.
E. arcuata has a mean body mass of 15.1±1.96 mg (N=8), which corresponds to a weight (Fm) of 1.48x10-4 N. Consequently, the adhesive force of E. arcuata is 160 times its weight when maximum contact with a surface is achieved.
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Discussion |
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However, an attachment system with such an organisation of setae and setules possesses an enormous adaptability to any given substrate and results in the largest possible contact area between the two. In particular, the setose elements, with setal lengths ranging between 100 µm and 280 µm, setule lengths of 34 µm, a setule stem diameter of 0.2 µm and the setule tip surface area of approximately 0.17 µm2 provide the geometrical features required for this high adaptability.
Fine-scale specialisation of tarsal elements to such a high degree is not
uncommon in arthropods, yet in E. arcuata it reaches a level that is
far more differentiated than so far described in other arthropods, e.g.
insects. Setal length in marmelade hoverfly Episyrphus balteatus
(Syrphidae), for example, measures merely 34 µm, with a stem diameter of
approximately 0.5 µm (Gorb,
1998), and setal branching is usually totally absent. Thus, E.
arcuata, with 624 000 contact points, ranges clearly higher than the data
documented for insects. When the latter possess setose structures beside their
tarsal claws and not just adhesive pads, as in, for example, the Aphidae,
Hymenoptera and Orthoptera, 500042 000 contact points were found in
E. balteatus and the blowfly Calliphora vomitoria,
respectively (Gorb, 1998
;
Walker et al., 1985
). Only
tortoise beetle Hemisphaerota cyanea, with its 120 000 points of
contact, reaches a comparable order of magnitude
(Attygalle et al., 2000
;
Eisner and Aneshansley,
2000
).
The number of contact points to the substrate in E. arcuata even
seems above average for Araneae. In zebra spider Salticus scenicus
(Salticidae), which is comparable in size and body mass, whole animals are
reported to have only 211 000 setules, with a terminal setule surface area of
only approximately 0.048 µm2
(Roscoe and Walker, 1991).
Consequently, the total adhesive area in S. scenicus is only about
10% of that in E. arcuata.
Besides a high number of contact points, a soft material is required to
conform to the substrate surface texture. Furthermore, in terms of material
behaviour, viscose as well as elastic properties are demanded in order to
attain an adequate number of attachmentdetachment cycles. To date, few
analyses of the mechanical properties of arthropod cuticle are available, in
particular as far as material hardness is concerned. The few documented
figures lie between 200 MPa and 400 MPa
(Hillerton et al., 1982;
Kreuz et al., 2000
). The far
better analysed material elasticity is distinguished by a high degree of
variability. Values between 103 Pa
(Vincent and Pentrice, 1973
)
and 1010 Pa (Jensen and
Weis-Fogh, 1962
) are stated for the Young's modulus of
Locusta cuticle. Even less data are available for chelicerates.
Recently, the rates of elasticity were determined for the alloscutum of the
tick Ixodes ricinus, with values ranging between 0.17 GPa and 1.5 GPa
(Seidl, 2002
). By integrating
the rubber-like protein resilin in defined locations, further functionally
adequate, high elasticities can be obtained in I. ricinus (Dillinger
and Kesel, in press). Providing that the cuticular material of the attachment
system possesses similar characteristics, it is supplied not only with the
structural elements but also with the material properties required for a
detailed reproduction of the substrate.
AFM analysis adhesion and tenacity
As expected, the elaborate attachment system of E. arcuata results
in a high adhesive force (2.4x105 N), with absolute values
similar to those documented for larger and heavier animals such as the
cockroach Periplaneta americana (Pell, cited in
Walker, 1993). Thus, the body
mass-related safety factor (SF; Fa/Fm) of
160 appears surprisingly high. Insects achieve factors of between 1.5 (P.
americana; Pell, cited in Walker,
1993
) and 50 (knotgrass leaf beetle Chrysolina polita;
Stork, 1980b
), although a
safety factor of 146 has been reported (cocktail ants Crematogaster
spec; Federle et al.,
2000
). In fact, the safety factor of E. arcuata is only
exceeded by that of the beetle Hemisphaerota cyanea, which is
temporarily able to adhere with a force 200 times its body mass (Attygale et
al., 2000). The adhesive tenacity (
) produced by insects is reportedly
between 2x103 N m-2 (great green bush cricket
Tettigonia viridissima; Jiao et
al., 2000
) and 8x104 N m-2 (H.
cyanea; estimated from Attygale et al., 2000). Significantly higher
values have been obtained when adhesive tenacity is measured parallel to
(
p) rather than normal (
n) to the contact
surface. Under these circumstances, additional friction forces contribute
considerably to adhesion. With an adequate experimental set-up, Walker
(1993
) registered a
p of 28.6x104 N m-2 for C.
vomitoria, which was ten times larger than
n
(2.9x104 N m-2). Thus, the
n
(2.24x105 N m-2) for E. arcuata, gained
by adhesion measurements perpendicular to a contact surface in the present
study, lies approximately one order of magnitude above that described for
insects. Comparably large adhesive capacities have, until now, only been
documented for geckoes. The gecko's attachment system is remarkably similar to
that of E. arcuata. Gecko adhesion is also made possible by a highly
structured attachment system of comparable dimensions, and the keratin contact
elements, the so-called spatulae, are also reported to be free of adhesive
secretions (Ruibal and Ernst,
1965
; Hiller,
1968
; Stork,
1983
). Although adhesive forces are not documented for single
spatulae, they are for single setae and, with a
of
5.76x105 N m-2, these range within the same order
of magnitude as measured here for E. arcuata
(Autumn et al., 2002
).
Analogous to the findings in Calliphora
(Walker et al., 1985
;
Walker, 1993
) and Syrphids
(Gorb et al., 2001
), it was
shown that a perpendicular preloading and subsequent pulling of the attachment
system parallel to the substrate surface dramatically enhances the adhesive
force in geckoes (Autumn et al.,
2000
). It can thus be concluded that friction forces dominate over
all other possible adhesive forces in any attachment system. Nevertheless, dry
adhesive mechanisms seem superior to wet adhesive mechanisms with regard to
the adhesive force perpendicular to surfaces.
The physical principle forming the basis for wet adhesion is surface
tension of an adhesive secretion between the attachment device and substrate
(Bauchhenß, 1979;
Walker et al., 1985
;
Dixon et al., 1990
;
Walker, 1993
). By contrast,
van der Waals forces have recently been discussed for the dry adhesive system
in geckoes (Autumn et al.,
2000
,
2002
). These short-ranged
forces are relatively independent of the materials in contact but demand close
proximity (only a few nanometres) of the contacting areas. The ultrastructural
design of the spider scopula shown here could allow such a close approach. As
previously mentioned, pointspectroscopy, as carried out in this study, is a
valid method for determining van der Waals forces
(Hartmann, 1991
). Thus, the
measured 38.12 nN were interpreted as the mean van der Waals force of a
single, isolated setule contact area. Admittedly, evidence still has to be
provided as to whether adhesion to a substrate results from van der Waals
forces in the living system.
In addition, it should be pointed out that the extremely high SF of 160 can
only be attained if all 624 000 setules are in full contact with the
substrate. This represents the upper limit. The same situation was observed in
geckoes, for which the high total adhesive force was calculated from single
seta measurements (Autumn et al.,
2000,
2002
). Experiments on live
animals provided significantly reduced figures, with a tenacity of only
8.7x104 N m-2
(Irschick et al., 1996
).
Analogous reductions can be expected for E. arcuata. Furthermore, the
hunting lifestyle, especially the associated dynamics, substrate
contamination, wear of the cuticular attachment devices and numerous other
factors should result in a drastic decrease in adhesion. Nonetheless, even a
significantly reduced SF should be sufficient to guarantee a secure grip on
smooth plant surfaces as well as successful prey capture. As behavioural
studies of salticids have shown, prey capture is even possible when hanging in
an upside-down position with some of the feet holding on to the substrate
while the other feet firmly cling to the prey.
The remarkable adhesive capacities presented for E. arcuata raise a final and important question: how does the spider detach its feet from a substrate? Although it is known that the animals do detach their front legs before jumping, a detailed study of the actual detachment process at the level of the scopula has yet to be performed. Further experiments are planned to address this issue.
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Acknowledgments |
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