van der Waals and hygroscopic forces of adhesion generated by spider capture threads
1 College of Veterinary Medicine, Virginia Tech, Blacksburg, VA 24061,
USA
2 Department of Biology, Virginia Tech, Blacksburg, VA 24061, USA
* Author for correspondence (e-mail: bopell{at}vt.edu)
Accepted 21 July 2003
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Summary |
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Key words: adhesion, capillary adhesion, cribellar thread, spider thread, Hypochilus pococki, Hyptiotes cavatus
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Introduction |
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Cribellar thread is a composite thread formed of internal supporting fibers
covered by a dense mat of several thousand small-diameter fibrils
(Fig. 1;
Hawthorn and Opell, 2002;
Opell, 1994a
,
1999
; Peters,
1984
,
1986
). Cribellar threads are
so named because these fibrils are spun from spigots of an abdominal spinning
plate (sometimes divided) called the cribellum (Opell,
1994a
,
1999
;
Peters, 1984
). These protein
fibrils are drawn from the cribellum by a setal comb on each of a spider's
fourth legs (Eberhard, 1988
;
Opell, 2001
;
Opell et al., 2000
) and formed
around larger, internal supporting strands
(Eberhard and Pereira, 1993
)
by adductions of the median spinnerets
(Peters, 1986
). The completed
thread often forms a series of regular puffs (Opell,
1994a
,
1999
; Peters,
1984
,
1986
). Thread stickiness is
determined by the number of fibrils that form its surface (Opell
1994a
,
1999
) and is modified by the
dimensions of puffs and the manner in which a spider loops and folds a
finished thread (Opell, 1995a
,
2002
).
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The appearance of cribellar thread is associated with the appearance of
aerial capture webs and corresponds to the origin of the Infraorder
Araneomorphae, which contains 95% of all living spiders
(Bond and Opell, 1998;
Coddington and Levi, 1991
).
Some araneomorph spiders have lost the ability to produce cribellar threads as
they have adopted other prey capture strategies and some have replaced
cribellar thread with viscous thread
(Coddington and Levi, 1991
;
Opell, 1997
,
1998
). Today, approximately
3606 species in 371 genera and 22 families spin cribellar threads
(Griswold et al., 1999
;
Platnick, 2000
). Of these,
only 11 species in two genera of one family produce primitive, cylindrical,
non-noded fibrils (Fig. 1B).
The remainder produce fibrils with regularly spaced nodes
(Fig. 1C; Hawthorn and Opell, 2002
;
Opell, 1994a
). The only
exceptions are members of the family Filistatidae, which produce derived,
flattened cribellar fibrils (Eberhard and
Pereira, 1993
).
Cribellar thread employs two stickiness mechanisms to hold a wide range of
insect surfaces (Opell,
1994b): mechanical interlock (snagging) and adhesion. The fibrils
on a thread's surface snag an insect's setae and hold them like the soft,
looped side of a VelcroTM fastener
(Opell, 1994b
). However,
cribellar thread also adheres to smooth surfaces such as graphite, polished
steel, glass and beetle elytra (Eberhard,
1980
; Opell,
1994b
) by uncharacterized mechanisms. Adhesion to smooth surfaces
can be achieved by van der Waals forces and electrostatic attraction (Allen,
1992a
,b
,c
).
Electrostatic attraction has been suggested for cribellar threads (Peters,
1984
,
1986
), but it has not been
supported experimentally (Opell,
1995b
).
van der Waals forces encompass two mechanisms: London dispersion forces and
hygroscopic adhesion. The former depends only on the presence of nuclei and
electrons and can operate between any two molecules that are in sufficiently
close proximity (Hobsa and Zahradnik,
1988). These weak interactions arise when an instantaneous dipole
in one molecule creates a synchronized instantaneous dipole in neighboring
molecules. Surfaces can attract at a distance of 50 nm
(Rigby et al., 1986
).
Hygroscopic adhesion, also known as capillary adhesion
(Autumn et al., 2002
;
Stork, 1980
), is generated
when a thin film of water sticks to surfaces by adhesive forces and to other
water molecules by cohesive forces, both of which involve hydrogen bonding. As
the forces of adhesion are usually stronger than those of cohesion, the
strength with which a water film holds surfaces together is determined by
surface tension (Stork, 1980
)
and Laplace pressure (Israelachvili,
1992
). It is not necessary for an organism to secrete this water,
as hydrophilic substances can attract atmospheric moisture
(Stork, 1980
). For example,
hydrophilic compounds in viscous capture threads attract atmospheric water to
increase the volume of their droplets
(Townley et al., 1991
).
In a recent study (Hawthorn and Opell,
2002), we demonstrated that, when tested with a smooth surface,
cribellar threads formed of non-noded fibrils registered the same stickiness
under low and high humidity. By contrast, threads formed of noded fibrils
registered greater stickiness under high humidity. These results support the
hypothesis that plesiomorphic cribellar threads formed of non-noded fibrils
employ only van der Waals forces of adhesion, whereas derived cribellar
threads formed of noded fibrils implement hygroscopic adhesion. The present
study uses an approach similar to that employed by Autumn et al.
(2000
,
2002
) to provide an additional
test of this hypothesis. Here, we model the forces of adhesion generated by
van der Waals and hygroscopic forces for cribellar threads formed of noded and
non-noded fibrils and compare these forces to the stickiness values measured
for cribellar threads under high and low ambient humidity.
Previous studies of thread adhesion (e.g. Opell,
1994a,b
,
1997
,
1999
) have reported stickiness
as the µN of force required to pull each mm length of thread from a contact
plate. These contact plates were made of fine sandpaper that yields the same
stickiness values as plates made from a fleshfly wing (Opell,
1994c
,
1997
) and were 1960-2040 µm
wide. This method was appropriate for the broad phylogenetic comparisons made
in these studies. However, the models that we wish to develop require us to
re-examine the way cribellar thread releases from a smooth surface. We believe
that as a smooth contact plate pulls away from a thread, force is concentrated
in a narrow band along each edge of the plate (Figs
2,
3). When this force overcomes
the thread's adhesive forces, the thread peels rapidly from the edges of the
plate towards its center, and the plate releases from the thread. To test this
hypothesis, we measured the force required to overcome thread stickiness with
narrow and wide contact plates. The hypothesis predicts that there should be
little difference between the values registered by these plates.
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Materials and methods |
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We measured the stickiness of some of these threads and photographed others under light and scanning electron (SEM) microscopes. Threads that were examined under the SEM were transferred to stubs and sputter coated with 4 nm of gold before being viewed at a magnification of approximately 100 000x. Low acceleration voltage of 2.00 kV prevented damage to the fibrils. Images of these fibrils and their included scale bars were saved digitally. Other threads were photographed under a dissecting microscope and a compound microscope equipped with differential interference contrast optics. These 35 mmslides were scanned to produce digital images. We measured these images of fibrils and threads with NIH Image and computed the number of point contacts between a thread and a smooth surface. We then used these data to model thread stickiness. Details of these procedures are described below.
Measuring thread stickiness
We measured thread stickiness with an instrument that incorporated a
stainless steel strain gauge with a 2000 µm-wide contact plate (±40
µ m) on its free end (Bond and Opell,
1998; Opell,
1994a
,b
,
1995a
,b
,
1997
,
1998
,
1999
,
2002
). A motorized advancement
mechanism pressed the plate against a thread at a speed of 10.4 mm
min-1 until a force of 19.61 µN was achieved. The thread was
then withdrawn at 10.7 mm min-1 until it pulled free of the plate
(Fig. 2). The needle's position
on a scale at the time of release was recorded, and the mass required to
deflect it to this position was multiplied by the accelerating force of
gravity to yield the force (in Newtons) required to pull the plate from a
thread. Under each humidity condition, we measured the stickiness of three
threads per spider and used the mean value as the stickiness of this spider's
thread at this humidity. Contact plates were surfaced with acetate from the
non-sticky side of Scotch MagicTM Tape 810 (3M Co., St Paul,
Minnesota, USA). This relatively nonpolar surface does not attract moisture,
and SEM examination shows it to be fairly smooth even at the scale of tens of
nanometers, at which the cribellar fibrils operate. Thus, we believe that
there is maximum contact between cribellar fibrils and this surface. At a
relative humidity (RH) of around 50%, noded cribellar thread sticks to this
surface with a force comparable to that with which it holds fleshfly wings
(Hawthorn and Opell, 2002
).
Thus, measured forces are in the range of those registered by a representative
insect surface.
This stickiness instrument was enclosed in a clear, Plexiglas box. Low humidity (under 3% RH) was achieved by flushing the box with nitrogen. A small electric fan in the chamber ensured thorough mixing of the atmosphere. High humidity (near 100% RH) was achieved by bubbling the nitrogen through distilled water before it entered the box and by placing a piece of cloth dampened with distilled water over the fan. We measured the humidity and temperature with a digital hygrometer thermometer, dew point instrument (model 11-661-7B; Fisher Scientific, Pittsburgh, Pennsylvania, USA). These values were recorded at the beginning and end of each of the three stickiness measurements taken of a spider's thread and the mean values were used as the humidity and temperature for that trial.
Measuring stickiness with narrow and wide plates
Three narrow plates (1500, 1530 and 1560 µm widths) and three wide
plates (2700, 2760 and 2760 µm widths) were prepared during the same
one-hour period. Enough threads were collected from each of the webs produced
by 13 adult female H. cavatus to permit four stickiness measurements
with narrow and wide places, except in two cases where only three measurements
were made with a plate of each width. Most threads were measured within 16 h
of being produced and all within 36 h of being produced. After the stickiness
of a series of threads from 2-4 webs was measured with a wide plate, the plate
was removed from the needle and replaced with a new narrow plate. The narrow
plate was then used to re-measure the first series of threads and then to take
measurements of the next series of threads before being replaced by a new wide
plate. In this fashion, stickiness measurements were alternated to control for
the age of threads and contact plates. Narrow plates were used to measure
stickiness under conditions (mean values: 23.1°C, 34.0% RH) similar to
those used for wide plates (mean values: 23.3°C, 35.4% RH).
Modeling data and calculations
To model thread stickiness, we first determined the number of contact
points (closely spaced points along non-noded cribellar fibrils and the nodes
of noded cribellar fibrils) within the bands of contact (two areas, each the
width of a flattened cribellar thread; Fig.
3) at the margins of contact plates. We then multiplied this total
by the adhesive forces computed for a single contact point. The details of
this process are described below.
The first step in modelling stickiness was to determine the number of nodes or contact points per thread area. For noded fibrils, we did this by determining the area of an SEM micrograph of cribellar thread, counting the number of nodes on the thread's surface fibrils (fibrils that were in sharp focus and not lying behind another fibril), and from these values computing node density. Thus, node density takes into account the coiled and stacked nature of the fibrils on the thread's surface. For H. cavatus threads, node density was 170±23 nodes µm-2 (N=5; all values are means ± S.D.).
We modeled the contact points of non-noded fibrils as a series of points separated by a distance of one fibril diameter. For H. pococki, the grand mean fibril diameter was 29±4.7 nm (N=6). The mean fibril diameter of each of these six individuals was calculated from the diameters of 10 fibrils from the cribellar thread. To determine the density of these contact points, we first measured the total length of the fibrils on a thread's surface that were in sharp focus and not overlain by other fibrils. We then divided this number by the total area of the micrograph to determine fibril density: 11 797±5222 nm µm-2 (N=6). Contact points are modeled as contiguous spheres whose diameters are equal to fibril diameter. Thus, the number of contact points along a fibril is equal to the fibril's length divided by its diameter. For H. pococki, this value is: 11 797 nm µm-2 divided by 29 nm = 407 contact points per µm2.
The second modeling step involved determining the width of a thread when it was pressed against the stickiness meter's contact plate. We did this by placing a glass cover slip on a cribellar thread that was held on the supports of a microscope slide sampler (described above) and examining under a compound microscope the thread sectors that were suspended between the supports. For H. cavatus threads, which are formed of regularly spaced puffs (Fig. 1A), we measured maximum puff width, which had a mean value of 209.9±35.5 µm (N=8).
Hypochilus pococki threads have a less regular outline. Therefore, we photographed these threads under a compound microscope when they were pressed against a cover slip. We then measured the contact surface area of a known length of thread and divided this by the length to determine the mean contact width of the thread sample. The mean thread contact area was 168±68.2 µm2 µm-1 (N=5) and the mean contact thread width was 168 µm.
In the third modeling step, we determined the areas of the two bands of contact between a cribellar thread and the upper and lower edges of a contact plate on the stickiness meter (Figs 2, 3). We computed the width of this band as the width of cribellar thread contacting a plate, and the length of the band as the diameter of one node or contact point plus the distance separating this point from an adjacent node or contact point. For H. cavatus, each band's width was the maximum width of a thread puff, and each band's length was a distance equal to one node diameter and one internode space (the distance between two adjacent fibril nodes) on either side of this node. We determined these values by first measuring 10 randomly selected nodes and internode spaces per thread, determining the mean per thread sample, and then computing the values of the grand means: node diameter = 35.3±1 nm (N=5), internode spacing = 85.5±7.2 nm (N=5). Thus, each band of contact had a width of 209.9 µm, a length of 0.121 µm and an area of 25.36 µm2. For H. pococki, each band's width was equal to the mean thread width, and each band's length was equal to the diameter of a contiguous spherical contact point (= fibril diameter). Thus, each band had a width of 168 µm, a length of 0.029 µm and an area of 4.872 µm2.
In the fourth modeling step, we determined the number of nodes or contact points in the contact bands of each species' threads. We did this by multiplying the area of contact by the node or contact point density. For H. cavatus, this value was: 25.36 µm2 x 170 nodes µm-2 = 4311 nodes per band of contact. For H. pococki, this value was: 4.872 µm2 x 407 contact points per µm2 = 1983 contact points per band of contact.
In the fifth step, we modeled the van der Waals force
(Fv) of a single point of contact as the force generated
by the contact between a sphere and a plane, as described by the equation:
![]() | (1) |
For H. cavatus, this computation was:
![]() | (2) |
![]() | (3) |
![]() | (4) |
![]() | (5) |
In the seventh step, we computed the total van der Waals forces exerted by both bands of contact. For H. cavatus, this computation is: 4.82x10-3 µN node-1 x 4311 nodes x 2 contact bands = 41.56 µN. For H. pococki, this computation was: 3.99x10-3 µN point-1 x 1983 points x 2 contact bands = 15.82 µN.
In the eighth step, we computed the total hygroscopic force exerted by both contact bands of H. cavatus threads: 8.36x10-3 µN node-1 x 4311 nodes x 2 contact bands = 72.08 µN.
In the ninth step, we computed the cumulative van der Waals and hygroscopic forces exerted by both contact bands of H. cavatus threads. This value is 41.56+72.08=113.64 µN.
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Results |
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Modeled and measured stickiness
Our simple mathematical models of van der Waals and hygroscopic forces
yielded stickiness values that fall within one-half of a standard deviation of
the measured values (Fig. 4).
This agreement supports the hypothesized operation of van der Waals forces of
adhesion in cribellar threads formed of non-noded fibrils and in threads
formed of noded fibrils under very low humidity. It also supports the
hypothesis that at high humidity noded fibrils achieve greater stickiness by
implementing hygroscopic forces of adhesion.
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Hygroscopic forces alone are sufficient to explain the adhesion of cribellar threads formed of noded fibrils at high humidity. Under this condition, modeling adhesion as the combination of van der Waals and hygroscopic forces greatly overestimates thread stickiness. Consequently, it appears that both of these forces do not act simultaneously and that hygroscopic forces replace van der Waals forces at high ambient humidity.
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Discussion |
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Primitive cribellar threads formed of cylindrical fibrils rely only on van
der Waals forces to stick to smooth surfaces
(Hawthorn and Opell, 2002).
Consequently, an increase in the stickiness of cribellar threads formed of
these fibrils requires an increase in the number of fibrils that contact a
surface. This can be achieved by increasing the number of spigots on the
cribellum (Opell, 1994a
,
1999
) or by configuring
cribellar threads so that more fibrils contact the surface
(Opell, 2002
). Either strategy
requires an increase in protein expenditure. The appearance of noded cribellar
fibrils was probably favored because it increased thread adhesion at most
ambient humidity conditions without requiring a proportional increase in
protein expenditure. As noded fibrils press against a smooth surface, it
appears that the nodes are the principal points of contact. Thus, nodes seem
to reduce the area of contact between fibrils and surfaces. This further
emphasizes the strength of adhesive forces that operate at the nodes. It is
presumably here that the hydrophilic regions of the silk reside.
Our models not only document the ability of cribellar threads to implement
van der Waals and hygroscopic forces but they also provide insights into the
operation and design of these threads. The peeling phenomenon on which our
models are based probably operates to some degree even on insect surfaces that
are covered by setae. Thus, the prominent cribellar thread puffs that
characterize capture threads spun by members of the orb-weaving family
Uloboridae (Opell,
1994a,b
,
1999
) may have been selected
to maximize thread efficiency. If thread stickiness is, to a large extent, a
measure of the threshold force necessary to overcome bands of adhesion along
the edges of a contact surface, then producing threads that are puffed rather
than of uniform width would represent an optimal expenditure of material.
Thread puffs maximize the widths of contact with the edges of a surface and,
consequently, the forces of adhesion generated in these areas. Narrower thread
regions between these edge areas of contact probably do not greatly reduce
thread stickiness, as these intermediate regions only experience force after
the peeling threshold of edge areas has been exceeded.
The nodes of derived cribellar fibrils may contribute to thread function in
additional ways. Nodes may make it more difficult for fibrils to slide over
one another when cribellar threads are being spun and after they have been
incorporated into webs. This would reduce the tendency for fibrils to pack
together and, thereby, allow more fibrils to contact a prey when it strikes
the web. Noded fibrils may also help absorb the force that is generated when
an insect strikes the web and as it struggles to free itself. They could do so
by offering more resistance than cylindrical fibrils to forces that cause
fibrils to slide over one another and to pull free from the larger supporting
fibers inside the thread. This resistance to sliding might also cause the
internode segments of fibrils to stretch and, thereby, dissipate additional
energy. A complete understanding of the functional properties of cribellar
threads awaits the characterization of the molecular architecture and
functional properties of their fibrils, such as is beginning to be done for
other types of spider silks (Gosline et
al., 1999; Guerette et al.,
1996
; Hayashi and Lewis,
1998
,
2000
;
Hinman and Lewis, 1992
).
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Acknowledgments |
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