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Phasmatodea (stick and leaf insects) are herbivorous insects well camouflaged on the plant substrates due to cryptic masquerade. Also their close association with plants makes them adapted to different substrate geometries and surface topographies of the plants they imitate. During past years, stick insects gained increasing attention in attachment- and locomotion-focused research. However, most studies experimentally investigating stick insect attachment have been performed either on single attachment pads or on flat surfaces. In contrast, curved surfaces, especially twigs or stems of plants, are dominant substrates for phytophagous insects, but not much is known about the influence of curvature on their attachment. In this study, by combining the analysis of the tarsal usage with mechanical traction and pull-off force measurements, we investigate the attachment performance on curved substrates with different diameters in two species of stick insects with different tarsal length. We provide the first quantitative data for forces generated by stick insects on convex curved substrates and show that the curvature significantly influences the attachment abilities in both species. Within the studied range of substrate curvatures, traction force decreases and the pull-off force increases with increasing curvature. Shorter tarsi demonstrate reduced forces, however, the tarsus length only has an influence for diameters thinner than the tarsal length. The attachment force generally depends on the number of tarsi/tarsomeres in contact, tarsus/leg orientation and body posture on the surface. Pull-off force is also influenced by the tibiotarsal angle, with higher pull-off force for lower angles, while traction force is mainly influenced by load, i.e. adduction force.
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RESEARCH ARTICLE
Attachment performance of stick insects (Phasmatodea) on
convex substrates
Thies H. Bu
̈scher*, Martin Becker and Stanislav N. Gorb
ABSTRACT
Phasmatodea (stick and leaf insects) are herbivorous insects well
camouflaged on plant substrates as a result of cryptic masquerade.
Also, their close association with plants has allowed them to adapt to
different substrate geometries and surface topographies of the plants
they imitate. Stick insects are gaining increasing attention in
attachment- and locomotion-focused research. However, most
studies experimentally investigating stick insect attachment have
been performed either on single attachment pads or on flat surfaces.
In contrast, curved surfaces, especially twigs or stems of plants, are
dominant substrates for phytophagous insects, but not much is
known about the influence of curvature on their attachment. In this
study, by combining analysis of tarsal usage with mechanical traction
and pull-off force measurements, we investigated the attachment
performance on curved substrates with different diameters in two
species of stick insects with different tarsal lengths. We provide the
first quantitative data for forces generated by stick insects on convex
curved substrates and show that the curvature significantly influences
attachment ability in both species. Within the studied range of
substrate curvatures, traction force decreases and pull-off force
increases with increasing curvature. Shorter tarsi demonstrate
reduced forces; however, tarsus length only has an influence for
diameters thinner than the tarsal length. The attachment force
generally depends on the number of tarsi/tarsomeres in contact,
tarsus/leg orientation and body posture on the surface. Pull-off force
is also influenced by the tibiotarsal angle, with higher pull-off force for
lower angles, while traction force is mainly influenced by load, i.e.
adduction force.
KEY WORDS: Adhesion, Friction, Biomechanics, Euplantula,
Arolium, Tarsal pads
INTRODUCTION
Attachment during locomotion on different kinds of surfaces is a
widespread phenomenon in the animal kingdom. Especially in
insects, various types of reversible attachment structures, which
allow them to hold themselves and to walk onthe majority of natural
surfaces (Beutel and Gorb, 2001, 2006, 2008), evolved in response
to the great variability of natural surfaces (Gorb, 2001; Gorb and
Gorb, 2004). Phasmatodea Jacobson and Bianchi 1902, or stick and
leaf insects, are a mesodiverse group of large terrestrial insects
(Bradler and Buckley, 2018) inhabiting various habitats worldwide
(Bedford, 1978; Brock et al., 2019). These herbivorous insects are
strongly adapted to foraging on plants, e.g. exhibiting extreme forms
of masquerade crypsis (Robertson et al., 2018), and presumably
have co-evolved with plants since pre-angiosperm times (Wang
et al., 2014). This process shaped the evolution of the attachment
apparatus of phasmids and resulted in diverse adaptations to
different surfaces in their habitats (Büscher et al., 2019). As a result,
the tarsal attachment apparatus of most stick insects consists of a
flexible chain of five tarsomeres, bearing two types of attachment
pads and two claws. The tarsal euplantulae, present on the proximal
four/five tarsomeres, are used to generate friction and withstand
shear forces, and the pretarsal arolium provides adhesion to
withstand pull-off forces (Labonte and Federle, 2013). On smooth
or micro-rough surfaces, these pads provide attachment due to
adhesion and friction forces, whereas on rough surfaces the claws
additionally achieve mechanical interlocking (Büscher and Gorb,
2019). Species-specific functional attachment microstructures
(AMS) are present on the euplantulae of stick insects and
correlate with the different substrates in their natural habitats
(Büscher and Gorb, 2017; Büscher et al., 2018a,b, 2019). These
structures are reported for at least one species to change during post-
embryonic development, in which the animals change their habitat
(Gottardo et al., 2015). Previous studies on the attachment
performance of stick insects have shown that euplantulae with
smooth AMS generate higher forces on smooth surfaces, whereas
nubby euplantulae are adapted to micro-rough surfaces (Bußhardt
et al., 2012; Büscher and Gorb, 2019).
Most studies on the attachment properties of stick insects have
focused on the performance of single attachment pads (Bennemann
et al., 2011; Bußhardt et al., 2012; Labonte and Federle, 2013;
Labonte et al., 2014) and examined the adhesive and frictional
components of attachment in detail. Other studies, focusing on the
attachment performance of whole stick insects, investigated the
combination of the different pads and claws and their contribution to
the overall attachment (Büscher and Gorb, 2019; Labonte et al.,
2019). In regard to measurements of actual attachment forces, these
studies are limited to investigations of (1) size dependence of
attachment in different instars of one species ofstick insects (Labonte
et al., 2019) and (2) complementary effects of different components
of the attachment apparatus in two other species (Büscher and Gorb,
2019). Labonte et al. (2019) have shown that during the ontogeny of
stick insects, adhesion scales with contact area in whole-animal
measurements, as attachment performance compensates for weight in
larger stick insects by the weight-related shear forces produced by
sliding of the pads. Büscher and Gorb (2019) investigated the use of
all tarsal attachment structures in two species and showed a flexible
usage of the attachment pads according to the animals orientation to
the substrate. This study revealed stronger attachment forces on rough
substrates by the contribution of claws and on smooth substrates by
the contribution of tarsal attachment pads.
Although they provide insight into the functionality of the whole
attachment system, all these studies have been carried out on flat
Received 8 April 2020; Accepted 20 July 2020
Department of Functional Morphology and Biomechanics, Institute of Zoology, Kiel
University, Am Botanischen Garten 9, 24118 Kiel, Germany.
*Author for correspondence (tbuescher@zoologie.uni-kiel.de)
T.H.B., 0000-0003-0639-4699; S.N.G., 0000-0001-9712-7953
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© 2020. Published by The Company of Biologists Ltd
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Journal of Experimental Biology (2020) 223, jeb226514. doi:10.1242/jeb.226514
Journal of Experimental Biology
surfaces. In nature, stick insects face a lot of differently structured
surfaces. In particular, curved surfaces, such as branches or twigs of
plants, are among the most abundant substrates for stick and leaf
insects (Bedford, 1978; Gottardo et al., 2015; Büscher et al., 2019)
and have even shaped the appearance of most stick insects (Bedford,
1978; Wang et al., 2014; Bradler and Buckley, 2018). Locomotion
on curved substrates implicates different mechanics in comparison
to upright walking on flat substrates. Previous studies on other
insects have examined some aspects of locomotion on twigs and
curved substrates. Studies of different insect species walking on thin
stems revealed several strategies of attachment, including the use of
pads, claws and additional structures on the tibia enabling
attachment to and propulsion along the stems (Gladun and Gorb,
2007; Bußhardt et al., 2014). Measurements of attachment forces
showed remarkable differences between the maximal forces on
curved surfaces and flat ones for beetles and true bugs (Bußhardt
et al., 2014; Voigt et al., 2017, 2019). In these studies, the measured
attachment forces were higher on rods in comparison to flat plates of
the same material. The attachment performance on curved substrates
is different for different radii of curvature in relation to the
dimensions of the animal, as it has been shown for frogs that traction
is dependent on the diameter of the cylinder the frog tries to ascend
(Bijma et al., 2016; Hill et al., 2018).
On smooth flat surfaces, it is known that wide tarsi generate
higher attachment forces than slender tarsi in Stenus rove beetles
(Betz, 2002), demonstrating an influence of tarsus geometry on
attachment performance. The performance on different diameters of
curved substrates should be dependent on the length of the
attachment system instead. The length of the tarsal chain might
have an effect on how many attachment pads can be brought into
contact with a curved substrate and can further influence the
orientation of the attachment pads on the substrate. Friction
experiments on the euplantulae of two species of stick insects
revealed frictional anisotropy for both smooth and nubby
euplantulae (Bußhardt et al., 2012). At a load of 500 µN, the
species Medauroidea extradentata and Carausius morosus both
show higher friction in the proximal direction (pull) than in the
distal direction (push). The diameter of the structure in relation to
the length of the tarsal chain determines how the tarsi can be placed
on it (Gladun and Gorb, 2007; Voigt et al., 2017) and, hence,
influences the orientation of the animal and the direction of the
forces acting on the attachment system.
In this study, we examined the attachment capability of stick
insects on surfaces with different levels of curvature. We measured
the pull-off and traction forces of the species Sungaya inexpectata
and Orestes mouhotii. These two species differ primarily in body
size and in the length of their tarsi (Büscher et al., 2019).
Specifically, we aimed to answer the following questions. (1) How
does the attachment system of stick insects perform in traction and
pull-off on curved substrates with different diameters? (2) Does the
length of the tarsus influence attachment ability on surfaces with
different degrees of curvature? (3) How do stick insects use the
tarsal attachment system during locomotion on curved substrates?
MATERIALS AND METHODS
Animals
The species Sungaya inexpectata Zompro 1996 and Orestes
mouhotii (Bates 1865) were chosen (Fig. 1), as their tarsi differ in
the length of the tarsal chain, but not in either their overall tarsal
morphology (see Fig. 2) or their euplantular microstructures
(Büscher et al., 2019). Females were selected to avoid differences
caused by sexual dimorphism. All animals examined in this study
were obtained from the laboratory cultures of the Department of
Functional Morphology and Biomechanics (Kiel University,
Germany). They were fed with leaves of bramble (Rubus spp.)
and hazel (Corylus avellana)ad libitum. All animals retained a
natural day/night cycle. Adult individuals with six intact legs and no
visible damage on the attachment pads (using light microscopy)
were used. All insects were weighed prior to the measurements to
the nearest 100 µg (AG204 Delta Range, Mettler Toledo,
Columbus, OH, USA). We used the same specimens for pull-off
and traction force measurements and measured their mass on the
particular day of the measurement. As the mass of the specimens
changed over the course of the experiment, the values reported
below correspond to the masses of the individual insects at the time
of the measurements.
Scanning electron microscopy
Tarsi of both species were cut off from adult females and fixed in
2.5% glutaraldehyde in PBS buffer for 24 h on ice on a shaker.
Afterwards, samples were dried in an ascending ethanol series,
critical-point dried and sputter-coated with a 10 nm layer of gold-
palladium. The samples were mounted on a rotatable specimen
holder (Pohl, 2010) and overview images were obtained using a
scanning electron microscope (TM3000, Hitachi High-technologies
Corp., Tokyo, Japan) at 15 kV acceleration voltage. The
micrographs were processed and measurements of the tarsal
segments were conducted using the software Photoshop CS6
(Adobe Systems Inc., San Jose, CA, USA). The tarsi were
visualized from the lateral view to measure the length of all
tarsomeres (see Fig. 2).
Substrate preparation
As substrates, we used custom-made tubes and plates of acrylic
glass. We used four tubes with diameters of 24.8, 11.9, 5 and
2.9 mm to provide substrates that correspond to different abilities of
the animals to embrace the tubes. These cylinders correspond to the
different geometric characteristics of twigs in the natural habitats,
O. mouhotii
S. inexpectata
Fig. 1. Species examined in this study. Adult females of Sungaya
inexpectata and Orestes mouhotii. Scale bar: 2 cm.
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RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb226514. doi:10.1242/jeb.226514
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but exclude parameters influencing attachment, like differing
roughness, stiffness or surface chemistry. For comparison, we
used a flat square plate of acrylic glass. All substrates were cleaned
with ethanol prior to the experiment. During the experiments, the
substrates were cleaned between measurements to remove potential
residuals of attachment pad fluids from the substrates. All substrates
had a length of 25 cm, in order to provide sufficient latitude for
horizontal pulling.
Force measurements
Attachment forces were measured with a BIOPAC model MP100
and TCI-102 system (BIOPAC Systems, Inc., Goleta, CA, USA),
connected to a 100 gforce transducer (FORT100, World Precision
Instruments, Sarasota, FL, USA). A horse hair was attached to the
force transducer and glued with Plasticine to the metanotum of the
stick insect. The attachment forces of the insects were measured in
the following two directions: vertically (pull-off force) and
horizontally (traction force).
Pull-off forces
Specimens of both species (S. inexpectata 1.18±0.26 g mean±s.d.,
N=14; O. mouhotii 0.91±0.22 g, N=14) were attached to the force
transducer as described above. To pull the insects off the substrate at
an angle of 90 deg, the force transducer was mounted on a
micromanipulator (DC 3001R, World Precision Instruments Inc.)
with the same setup described by Wohlfart et al. (2014) and
employed for stick insects by Büscher and Gorb (2019). One glass
tube at a time, or the flat plate, respectively, was fixed below the
animal using two clamps. The micromanipulator was manually
moved upwards, with a retraction velocity of 24cms
1
, and
stretched the horse hair in the vertical direction until the animal
detached from the surface (see Fig. 3B).
Traction forces
Specimens of both species (S. inexpectata 1.32±0.31 g, N=14;
O. mouhotii 1.05±0.13 g, N=14) were attached to the force transducer
in the same manner as described above. To measure passive traction
force, the force transducer was aligned horizontally at the same height
as the insect (see Wolff and Gorb, 2012; Büscher and Gorb, 2019).
Each insectwasthen manually pulled backwards (along its bodyaxis)
in the traction direction without detaching it from the surface with a
retraction velocity of 25cms
1
(see Fig. 3A). As both species
preferred to walk upright on the flat surface and on the tube with the
largest diameter, but walked hanging upside down on the other tubes,
the traction forces were measured in accordance with the naturally
preferred animal orientation (see below).
O. mouhotii S. inexpectata
Total length (mm)
2
3
4
5
6
7
8
9*
Ta1
Ta2 Ta3 Ta 4
Ta5
Pt
Eu1 Cl
Ar
Cl
Cl
Ar
Cl
Eu2 Eu3 Eu4 Eu5
Eu1 Eu2 Eu3 Eu4 Eu5
A
B
C
D
E
F
Fig. 2. Tarsal morphology of the examined species. (AC) Scanning electron micrographs of the right metatarsus of an adult female O. mouhotii (A,B) and
Sungaya inexpectata (C) (A, lateral overview; B,C, ventral overviews). (D) Total tarsal length of the two species ( paired t-test, t=24.26, d.f.=10, N
1,2
=11,
P<0.001). Boxes indicate the 25th and 75th percentiles, whiskers are the 10th and 90th percentiles and the line within the boxes shows the median. (E,F) The
nubby microstructure on the euplantulae (4th euplantula) of the right metatarsus of an adult female O. mouhotii (E) and S. inexpectata (F). Ar, arolium; Cl, claw;
Eu, euplantula; Pt, pretarsus; Ta, tarsomere. *P<0.001. Scale bars: 1 mm (AC), 4 µm (E,F).
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Force data analysis
In both directions, forcetime curves were recorded and visualized
with the software Acqknowledge 3.7.0 (BIOPAC Systems Inc.,
Goleta, CA, USA). The maximum peak of the forcetime curve was
extracted for data analysis (see Fig. 3C,D for example curves). For
every direction and every species, the attachment forces for 14
individuals were measured. Every insect was measured 3 times and
the median of all three maximum attachment forces was taken. The
order of surfaces was randomized for each animal and the order of
measured individuals was also randomized during the experiment.
All measurements were performed in daylight at 1921°C and 50
60% relative humidity. Additionally, the behaviour of animals was
documented during the measurements.
Videography
To evaluate walking behaviour and leg positioning, adult females of
both species were filmed on each surface (S. inexpectata 1.24±
0.27 g, N=10; O. mouhotii 1.04±0.13 mg, N=10). The animals were
filmed with a Nikon D5300 digital camera (Nikon Corp., Tokyo,
Japan) equipped with a macro lens (Canon Macro Lens EF 100 mm,
Canon Inc., Tokyo, Japan) from the lateral side on all substrates. We
analysed (1) the walking gait pattern, (2) the orientation of the
specimen in relation to the substrate and (3) the positioning of the
tarsi. Therefore, sequences of at least 10 steps were analysed and
sequences with disruptions (turns, falls, etc.) were excluded. For the
flat substrate, only sequences where the animal walked in a straight
line were used. For analysis of the videos, Adobe Premiere Pro CS6
software (Adobe Systems Inc.) was used. To evaluate the walking
gait patterns, three general patterns were identified (tripod,
quadrupedal/tetrapod, waive gait; see Grabowska et al., 2012;
Büscher and Gorb, 2019), based on the number of feet
simultaneously in contact with the substrate, with a maximum of
10% of steps deviating from the ground pattern. If more than 10% of
steps were observed differing from the ground pattern (e.g.
transitions between two gait patterns), we considered these gait
pattern sequences as irregular.
Statistical analysis
SigmaPlot 12.0 (Systat Software Inc., San Jose, CA, USA) was used
to perform the statistical analyses. Initially, normal distribution
(ShapiroWilk test) and homoscedasticity (Levenes test) were
tested. The tarsal length and the body weight of both species were
compared using a two-tailed t-test. The traction and pull-off forces
on the five different substrate radii were compared for both species
separately using one-way ANOVA and HolmŠidákspost hoc test,
if the data were normally distributed and showed homoscedasticity.
KruskalWallis ANOVA on ranks and Tukeyspost hoc tests were
used if the data were not normally distributed. The safety factors
(attachment force per body mass) of the two species on substrates
with different radii were compared using t-test. For better
understanding, the exact test used and the sample size are
specified in the relevant sections.
RESULTS
Tarsal morphology
As for the majority of extant Phasmatodea, the tarsi of both species
examined consisted of five tarsomeres (see Büscher et al., 2019),
each equipped with one euplantula (Fig. 2AC). The pretarsus bears
two claws and an arolium. The tarsi of S. inexpectata were
significantly longer than the tarsi of O. mouhotii ( paired t-test,
t=24.26, d.f.=10, N
1,2
=11, P<0.001). The measurements of the
length of single tarsomeres and the total length of the tarsus in all
specimens are available in Table S1. We did not find significant
differences in the total tarsal length between different leg pairs in the
d1
d2
d3
d4
d5
d=24.8 mm
d=11.9 mm
d=5.0 mm
d=2.9 mm
Flat
A
B
EC
D
Time (s)
mtf
mpf
0 5 10 15 20 25 30
0
0
20
40
60
80
100
120
0
50
100
150
200
5 101520253035
Traction force (mN)Pull-off force (mN)
Fig. 3. Experimental setup for traction and pull-off force measurements. (A,B) Schematic setup of force measurements in the traction (A) and
pull-off (B) direction.(C,D) Example curves for traction (C) and pull-off force (D).(E) Cross-sections of the flat plate (d
1
) and cylindrical substrates used in the
experiments: 24.8 mm (d
2
), 11.9 mm (d
3
), 5 mm (d
4
) and 2.9 mm diameter (d
5
) tube. mtf, maximum traction force; mpf, maximum pull-off force.
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two species examined (see Table S2; S. inexpectata: KruskalWallis
one-way ANOVA; H=2.455, d.f.=2; P=0.293, N=15; O. mouhotii:
KruskalWallis one-way ANOVA; H=0.0614, d.f.=2, P=0.97,
N=15). The total length of the S. inexpectata tarsus (all three leg
pairs pooled) was 7.87±0.36 mm (median±s.d.) and 3.47±0.34 mm
for O. mouhotii (see Fig. 2). The major difference in the
tarsal morphology between both species was the length of the
single tarsomeres. In particular, the basitarsus (Ta1) was longer in
S. inexpectata (2.91±0.13 mm) than in O. mouhotii (1.0±0.1 mm).
Both species possess a nubby microstructure on the euplantulae (see
Fig. 2), as previously reported (e.g. Büscher et al., 2019). Although
the length of the tarsi of the same leg pairs differed between the
species, the dimensions of the surface microstructure on the
euplantulae were similar (Fig. 2E,F).
Locomotion on curved substrates
The locomotory behaviour on the test substrates differed depending
on the degree of their curvature. All tested individuals were analysed
to obtain the following data: (1) walking gait pattern, (2) orientation
on the substrate, (3) angle of attachment (AoA) and (4) leg
configuration (see Fig. 4). The AoA is defined by the centre of the
animal in the frontal projection and the distal-most part of the tarsus
being in contact with the substrate (Fig. 4A). Both species showed
rather similar behaviour on each test substrate (Table 1). On nearly
all substrates, insects employed a tripod walking gait pattern (three
legs at once in swing phase). Only on the tube with the smallest
diameter did O. mouhotii walk more slowly and just moved two legs
at once (tetrapod gait) in 80% of the recorded sequences. The same
species used tripod gait in 100% of the sequences on all other
substrates except the tube with the largest diameter, where it used
tetrapod gait in 25% of the sequences. Sungaya inexpectata used
tripod gait less often, but still in the majority of sequences (Table 1).
On the smallest tube (2.9 mm diameter), S. inexpectata moved more
carefully and used tripod gait in only 40% of the sequences and
tetrapod gait in all of the others. On both the 5.0 and 24.8 mm tubes,
tripod gait was used in 90% of the sequences and on the flat
substrate in 60% of the sequences. All S. inexpectata sequences
which did not show tripedal walking gait patterns revealed
tetrapedal gait patterns.
The same orientation to the substrate was recorded in all
individuals of both species. On the 24.8 mm tube, both species
walked upright on the tube, attaching at an AoA of <90 deg
(Fig. 4B). On the three other tubes, both species walked hanging
upside down. This agrees to observations on the species Aretaon
asperrimus (Frantsevich and Cruse, 1997), which is quite closely
related to the species examined herein (Brock et al., 2019). While S.
A
B
d=24.8 mm d=11.9 mm d=5.0 mm d=2.9 mm
d=24.8 mm d=11.9 mm d=5.0 mm d=2.9 mm
C
E
G
D
F
H
<90 deg >90 deg >180 deg >180 deg
<90 deg <90 deg =90 deg >90 deg
Fig. 4. Posture and leg conformations of both species on the different substrates. (A,B) Body and leg positioning on the different substrate diameters (d)in
(A) O. mouhotii (short tarsus) and (B) S. inexpectata (long tarsus). AoA, angle of attachment, i.e. angle between the centre of the animal (in frontal
projection) and the distal-most part of the tarsus (indicated below each animal scheme). (CH) Images of example tarsal contacts taken in experiments:
S. inexpectata on d=2.9 mm (C); O. mouhotii on d=2.9 mm (D), d=5.0 mm (E), d=11.9 mm (F,G); and (H) S. inexpectata on d=11.9 mm.
Table 1. Walking pattern and body posture on the test substrates
Substrate diameter (mm)
Sungaya inexpectata Orestes mouhotii
Gait pattern Body posture Gait pattern Body posture
2.9 Tripod (40%) Tetrapod (60%) Hanging down Tetrapod (80%) Irregular (20%) Hanging down
5.0 Tripod (90%) Tetrapod (10%) Hanging down Tripod (100%) Hanging down
11.9 Tripod (100%) Hanging down Tripod (100%) Hanging down
24.8 Tripod (90%) Tetrapod (10%) Standing Tripod (75%) Tetrapod (25%) Standing
Plane Tripod (60%) Tetrapod (40%) Standing Tripod (100%) Standing
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inexpectata attached at the downside of the 11.9 mm tube at an AoA
of <90 deg, O. mouhotii revealed AoAs of >90 deg on the same
tube. On the smaller tubes, O. mouhotii embraced the tubes with
higher AoAs than S. inexpectata as well. While O. mouhotii
attached with AoAs of >180 deg on both 5.0 and 2.9 mm diameter
tubes, S. inexpectata revealed AoAs of 90 deg on 5.0 mm and
>90 deg but <180 deg on the 2.9 mm tube. While hanging down,
both species attached with AoAs of >90 deg on all substrates with
one exception: on the tube with a diameter of 11.9 mm,
S. inexpectata did not embrace the tube, but attached hanging on
the downside. Although the animals kept some distance from the
tube while hanging down, their legs were still angled (tibiofemoral
joint 90160 deg). In this posture, only the arolia were employed for
attachment (Fig. 4H). In all other situations in which the animals
were hanging upside down (11.9 mm for O. mouhotii, 5.0 and
2.9 mm for both species), the insects embraced the tubes with AoAs
of 90 deg or more. In these postures, animals employed all
attachment pads (arolia and euplantulae), except for the fifth
euplantula (see Fig. 2AC), which was used in only a few
sequences: on the 5 and 2.9 mm substrates by S. inexpectata and
only on the 2.9 mm substrate by O. mouhotii (Fig. 4CG). The four
proximal euplantulae were used on all curved substrates by both
species, except for all individuals of S. inexpectata, which used the
arolium only on the 11.9 mm substrate (Fig. 4H) and the arolium
and the distal-most three euplantulae on the 2.9 mm substrate.
Generally, on the flat substrate, both species brought only the
arolium and euplantulae of the third and fourth tarsomeres into
contact.
Traction forces
The traction forces, measured via horizontal pulls, revealed lower
values for smaller tube diameters for both species. Generally,
S. inexpectata showed the highest traction force (Fig. 5C) on the
24.8 mm diameter tube (272.38±111.40 mN , median±s.d.), lower
force on the flat substrate (230.05±97.87 mN) and further
decreasing values on decreasing tube diameters (11.9 mm:
220.17±77.92 mN, 5.0 mm: 146.07±53.67 mN, 2.9 mm: 126.97±
67.06 mN). Statistical analysis, however, revealed significant
differences primarily between the traction forces on larger tube
diameters and the flat substrate in comparison with smaller tube
diameters (one-way ANOVA, F=7.3, N=14, P<0.001). In detail, the
traction forces on the smallest tube (2.9 mm diameter) were
significantly lower than those on the flat substrate (HolmŠidák
test, P=0.015), the 24.8 mm diameter tube (HolmŠidák test,
P<0.001) and the 11.9 mm diameter tube (HolmŠidák test,
P=0.032), but not different from those on the 5.0 mm diameter
tube (HolmŠidák test, P=0.798). The traction forces generated on
the 5.0 mm diameter tube were significantly lower in comparison to
those on the largest tube (HolmŠidák test, P=0.002).
A similar trend was observed in O. mouhotii (Fig. 5A), with the
highest mean traction forces of 210.21±71.96 mN on the 24.8 mm
diameter tube, 188.28±90.47 mN on the flat substrate, 177.97±
d1
d2
d3
d4
d5
d=24.8 mm
d=11.9 mm
d=5.0 mm
d=2.9 mm
Flat
E
A
BD
C
Traction force (mN)
d1d2d3d4d5
d1d2d3d4d5
d1d2d3d4d5
d1d2d3d4d5
Substrates
0
100
200
300
400
500
600
0
100
200
300
400
500
600
0
50
100
150
200
250
300
Pull-off force (mN)
0
50
100
150
200
250
300
a a
b b b
a
cb,c
a,b a,b
b b
aaa
a
c
b b b
Traction
Pull-off
Fig. 5. Traction and pull-off force for the two species on the differently curved substrates. (A,B) Orestes mouhotii (N=14) traction force (A) and
pull-off force (B). (C,D) Sungaya inexpectata (N=14) traction force (C) and pull-off force (D). Groups with different lowercase letters are statistically different. Boxes
indicate the 25th and 75th percentiles, whiskers are the 10th and 90th percentiles and the line within the boxes shows the median. (E) The different substrates.
6
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb226514. doi:10.1242/jeb.226514
Journal of Experimental Biology
65.08 mN on the 11.9 mm diameter tube and 93.20±37.48 mN on
the 5.0 mm diameter tube. The lowest traction force of 60.12±
31.74 mN was measured on the 2.9 mm tube. In general,
O. mouhotii generated higher traction on the substrates with the
largest diameters (i.e. lowest curvature) and lower traction on the
smallest diameter tube. KruskalWallis one-way ANOVA
(H=41.82, d.f.=4, N=14, P=0.001) revealed a significantly higher
traction force on the flat substrate and the two largest tubes
(24.8 mm diameter and 11.9 mm diameter) in comparison to the
5.0 mm and 2.9 mm tubes (Tukeys test, P<0.05).
Pull-off forces
The pull-off forces generated by S. inexpectata (Fig. 5D) were
highest on the 5.0 mm tube with 166.41±34.93 mN (mean±s.d.)
(one-way ANOVA, F=30.65, N=14, P<0.001; HolmŠidák test,
P<0.001). The performance on this tube was significantly higher
than on the other tubes (2.9 mm: 99.73±37.57 mN, 11.9 mm:
119.61±26.39 mN, 24.8 mm: 98.08±33.02 mN), which were not
significantly different from each other (one-way ANOVA, F=30.65,
N=14, P<0.001; HolmŠidák test, P>0.05). The pull-off forces on
the flat substrate were significantly lower than on all other substrates
(40.14±17.42 mN; one-way ANOVA, F=30.65, N=14, P<0.001;
HolmŠidák test, P<0.001). For O. mouhotii, the pull-off forces
(Fig. 5B) were significantly higher on the three smallest tubes than
on the largest diameter tube and the flat substrate (2.9 mm: 111.68±
50.94 mN, 5 mm: 129.49±47.87 mN, 11.9 mm: 125.96±61.62 mN;
KruskalWallis ANOVA on ranks, H=40.05, d.f.=4, P0.001,
N=14; Tukeys test, P<0.05). The median of the pull-off forces was
highest on the 5.0 mm diameter tube, similar to S. inexpectata, but
the difference between the forces on 5.0 mm and the other small
substrate diameters was not significant (Tukeys test, P>0.05). The
mean pull-off force on the 24.8 mm diameter tube (67.41±
31.30 mN) was higher than that on the flat substrate (35.27±
14.62 mN); however, this difference was also statistically not
significant (KruskalWallis ANOVA on ranks, H=40.05, d.f.=4,
P0.001, N=14; Tukeys test, P>0.05). In contrast to the traction
forces, both species revealed increasing pull-off forces on
decreasing tube diameter, with the maximum on the 5.0 mm tube
and decreasing pull-off forces for tubes thinner than 5.0 mm.
Comparison of attachment forces between species
The adult females of O. mouhotii (0.91±0.22 g, N=14) were lighter
than those of S. inexpectata (1.18±0.26 g, N=14; t-test, t=3.09,
d.f.=13, P=0.009). Therefore, for comparing traction and pull-off
forces of the two species with different tarsal lengths, safety factors
(attachment force/body weight) were used (Fig. 6A,B). The safety
factor in the traction direction was higher for S. inexpectata (9.17±
4.13) in comparison to O. mouhotii (5.89±3.22) on the 2.9 mm tube
(t-test, t=2.337, d.f.=26, N
1,2
=14, P=0.014). On all other substrates,
the differences between the specific safety factors were not
0
10
20
30
40
50
0
5
10
15
20
25
30
A
B
d=24.8 mm
d=11.9 mm
d=5.0 mm
d=2.9 mm
Flat
Sungaya inexpectata
Orestes mouhotii
Substrates
Traction
Pull-off
Safety factorSafety factor
*
*
d1d2d3d4d5
d1d2d3d4d5
d1
d2
d3
d4
d5
Fig. 6. Comparison of safety factors in the traction and pull-off direction between the two species on the differently curved substrates. (A) Traction
(N=14 for both). (B) Pull-off (N=14 for both). Boxes indicate the 25th and 75th percentiles, whiskers are the 10th and 90th percentiles and the line within
the boxes shows the median. *P<0.05, only significant comparisons are displayed. (C) The different substrates.
7
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb226514. doi:10.1242/jeb.226514
Journal of Experimental Biology
significant. In contrast, comparison of safety factors in the pull-off
direction revealed a significantly higher safety factor on the 2.9 mm
tube for O. mouhotii (t-test, t=2.149, d.f.=26, N
1,2
=14, P=0.021)
(Fig. 6B). Although the safety factors in the pull-off direction on the
11.9 mm diameter tube were different for the species (O. mouhotii:
14.27±5.89, S. inexpectata: 11.05±4.12), the t-test probability value
was slightly higher than 0.05 (t-test, t=1.666, d.f.=26, N
1,2
=14,
P=0.054).
DISCUSSION
Tarsal morphology
In some stick insect species, the length of the tarsi differs between
the three leg pairs (Poinar, 2011; Vallotto et al., 2016, measured
from fig. 2 therein). We did not find a significant difference in the
total tarsal length between different leg pairs in the two species of
Heteropterygidae examined herein, but difference occurred between
the species. In the following, we discuss the functional relevance of
the different tarsal lengths in regard to the attachment performance
on curved substrates. Other insects use tibial spurs for locomotion
on curved substrates, either for interlocking with the stem (Gladun
and Gorb, 2007) or in combination with the pretarsal claws to
generate traction even on smooth curved substrates (Bußhardt et al.,
2014). Such structures are not present in the species examined
herein.
Attachment performance on curved substrates
In the vertical direction, the generated pull-off force of both species
increased with the degree of curvature, from the flat substrate to the
5.0 mm diameter tube. On the thinnest tube, the pull-off forces were
again reduced (see Fig. 4B,D). Accordingly, there is an optimal
range of stem diameter, where the stick insect generates the strongest
attachment, and despite the different tarsal lengths, this range was
surprisingly similar for the two species. Furthermore, in both
species, the generated pull-off force on the three smallest tubes, even
on the thinnest one (2.9 mm diameter), was significantly higher than
that on the flat plate.
On curved substrates, the increasing attachment performance can
be caused by generation of active adduction forces. When climbing
on thin rods, compared with their own body size, animals can utilize
clamping grips and generate active adduction forces to increase
normal load on the surface. This has been shown for tree frogs
(Endlein et al., 2017; Hill et al., 2018) and was additionally assumed
for sawyer beetles (Voigt et al., 2017) and other insect species from
different lineages (Gladun and Gorb, 2007). The angle between the
substrate surface and the direction of pulling obviously influences
the pull-off force. According to Kendalls peeling model, the
pulling force is dependent on the peeling angle (Kendall, 1975).
Insect attachment systems are usually more complex than Kendalls
classical peeling model predicts (Gorb and Heepe, 2017; Heepe
et al., 2017); still, there is a significant influence of the angle
between substrate and the detaching tarsus in many animals (Gu
et al., 2016). The relationship between peeling angle and attachment
force has been previously shown in Hymenoptera (Federle et al.,
2001), Diptera (Niederegger et al., 2002) and Blattodea (Clemente
and Federle, 2008), as well as in vertebrates, such as geckos
(Autumn et al., 2000; Persson and Gorb, 2003) and frogs (Hanna
and Barnes, 1991).
In the species examined herein, leg and tarsus orientation on a
curved tube caused a lower angle between the attachment pads and
the direction of pulling with increasing curvature of the substrate
(Fig. 4), resulting in a higher amount of force, which is necessary for
detachment of the attachment pad. This relationship is also reflected
by the AoA: a larger AoA of the animal on the substrate results in
more individual attachment pads in contact with the surface, with
the pulling force acting at a correspondingly lower angle.
Consequently, a higher AoA results in a higher pull-off force,
except for the smallest tube. The pull-off force on the smallest tube
(2.9 mm diameter) was significantly lower than on the 5.0 mm
diameter tube in S. inexpectata (in O. mouhotii, the median of the
pull-off force was lower as well, but not statistically significant).
Additionally, the walking gait pattern of both species revealed a
larger percentage of the tetrapod gait. The tetrapod gait in
comparison to the tripod gait often indicates a less secure
attachment to the substrate in insects (Gorb and Heepe, 2017;
Büscher and Gorb, 2019). On curved substrates with a very low
diameter, the flexion of the tarsal chain is not sufficient to bring all
attachment pads into contact with the substrate and hence results in a
lower pull-off force. However, S. inexpectata is able to contact the
2.9 mm diameter tube with the arolium and two euplantulae
(Fig. 4C).
In contrast to the pull-off forces, the traction forces were higher
for larger tube diameters and decreased with decreasing tube
diameter for both species (Fig. 5A,C). The traction forces were
highest on curved substrates with large diameters (24.8 mm). The
curvature of the substrate potentially enables the tarsi to better adapt
to the surface profile than on flat substrates. Additionally, the
convex substrate curvature provides better grasping of the substrate
and the generation of higher load on the tarsi in comparison to flat
substrates (Frantsevich and Cruse, 1997; Gladun and Gorb, 2007;
Voigt et al., 2017). On very thin stems, with similar or lower
diameter than the tarsal length, the examined species provide lower
traction force than on surfaces with a lower degree of curvature.
Generally, on the smaller tubes, especially on the thinnest ones,
fewer attachment pads were brought into contact and, hence, less
actual contact area was provided, resulting in lower attachment force
(Arzt et al., 2003; Persson and Gorb, 2003). Presumably, on smaller
diameter tubes, less contact area is available to distribute the
resulting forces, especially in the lateral dimension. This probably
results in a reduced stabilization on the thinner tubes in comparison
with the larger ones, leading to a faster detachment of single legs
and a lower attachment force in general. Additionally, in animals
that clamp their tarsi around the tubes, the traction force vector along
the substrate is oriented perpendicular to the orientation of the
tarsus. Accordingly, the tarsi are sliding in the lateral direction in
most cases. If the tarsi were arranged differently, the animals
actively positioned them along the tube and tried to counteract the
pulling direction. Previous studies have reported higher friction for
stick insect euplantuae while being pulled compared with being
pushed (Bußhardt et al., 2012). In the lateral direction of the
euplantula, to the best of our knowledge, nothing is known about the
frictional properties of the attachment pad in stick insects. The
generated traction force, however, is significantly lower on the
smaller tubes, where the tarsi cannot be arranged along the tube
length, in comparison to the flat substrate and the tubes with larger
diameters (Fig. 5A,C).
Influence of tarsal length on attachment on curved
substrates
In both directions (vertical and horizontal pulling), the two species
showed similar trends, i.e. higher pull-off force on thinner stems and
higher traction on thicker stems and flat substrates. The safety
factors of both species were similar and not statistically different on
all substrates except the 2.9 mm diameter tube. Hence, the length of
the tarsus essentially does not matter for stems with larger diameters
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Journal of Experimental Biology
than the tarsal length. Only on the thinnest tube (2.9 mm diameter)
was the safety factor of S. inexpectata in the traction direction higher
than for O. mouhotii and lower in the pull-off direction (Fig. 6). The
shorter tarsi of O. mouhotii can generate a larger AoA in comparison
to the longer tarsi of S. inexpectata. This results in a lower angle
between the tarsus and tibia and, hence, could explain the higher
safety factor of O. mouhotii in the pull-off direction (e.g. Gu et al.,
2016). In spite of the longer tarsus of S. inexpectata, it does not
allow for a proper grasping around the rod, as the tarsus is not
flexible enough to follow the perimeter of the substrate. The tarsus
of O. mouhotii, however, is able to bring all attachment pads into
contact.
Opiliones (Arachnida), or harvestmen, are able to provide friction
using their elongated and highly articulated prehensile feet (Wolff
et al., 2019). In contrast to harvestmen, stick insects, like most other
insects, are not able to hyperflex the tarsus and therefore need to
provide load by the coordinated action of contralateral legs (Gladun
and Gorb, 2007; Bußhardt et al., 2014; Voigt et al., 2017). The
safety factor in the traction direction was higher for S. inexpectata
on the substrate with the smallest diameter. The tarsi of this species
made contact with the substrate at a lower AoA than those of O.
mouhotii (Fig. 4), i.e. >90 deg but <180 deg. This results in
potentially better clamping and higher adduction forces of the
contralateral legs, and consequently, higher traction, as the traction
is dependent on the load on the attachment pads (e.g. Gorb and
Scherge, 2000; Gorb et al., 2000; Bußhardt et al., 2012; Gorb, 2007;
Labonte and Federle, 2013; Labonte et al., 2014). In O. mouhotii,in
contrast, the high AoA (>180 deg) on the small tube results in lower
adduction forces, as the tarsus grasps around the tube. The force
transmitted to the attachment pads is, in this conformation, not
generating load, as the tarsus is under tension. This is in agreement
with observations previously made on other insects, which clasp
stems with an equal or slightly larger diameter than the tarsal length,
but clutch stems with a smaller diameter with the contralateral tarsi
(Gladun and Gorb, 2007), and, as shown for the two species
examined herein, this clutching results in higher traction.
Usage of the attachment system for locomotion on curved
substrates
According to Federle and Endlein (2004), attachment is regulated
on four different hierarchical levels, ranging from control of the
attachment system itself, over movements of the tarsomeres/tarsi and
the legs, to the body kinematics. Some aspects of the tarsus, leg and
body positioning have already been discussed above. Furthermore,
there are some behavioural aspects influencing body kinematics in
addition to the walking gait patterns and posture (Table 1). Generally,
the clamping efficiency is dependent on morphological
characteristics; for example, the ratios of body width and leg length
(Voigt et al., 2017). The same ratios are reported to show a correlation
of behaviour and morphology, i.e. while climbing on stairs, stick
insect species with shorter legs show different behaviour from species
with long legs (Theunissen et al., 2015).
With respect to their body lengths, the legs of S. inexpectata are
longer than those of O. mouhotii. Both are associated with low-
growing vegetation and show quite similar feeding habits and bury
their eggs in the soil (Büscher et al., 2019). However, there are no
studies that have investigated details of their natural behaviour in the
field. Still, the tarsi of O. mouhotii are shorter and therefore perform
better on thin branches than those of S. inexpectata. Presumably, the
tarsi of O. mouhotii are adapted to locomote on low-growing
vegetation with small stem diameter, rather than larger plant
diameters (bushes and trees).
In lizards (Goodmann et al., 2008) and Stenus rove beetles (Betz,
2006) limb length and habitat correlate in some species, e.g. limb
length increases with perch diameter or habitat openness ( presence
of less suitable refugia in the habitat). Likewise, openness in the
natural habitats could be higher for S. inexpectata than for O.
mouhotii and therefore longer legs (and tarsi) could be a result of the
presence of larger substrate diameters and less-suitable twigs for
imitation in the natural habitats of S. inexpectata.
Ground-dwelling spiders with longer legs walk faster on curved
substrates with large diameter compared with flat substrates and thin
stems (Prenter et al., 2010). Similarly, S. inexpectata has longer
limbs and does not show any cataleptic defensive reaction and
instead tries to escape. Orestes mouhotii in contrast relies on its
camouflage in combination with thanatosis (Bedford, 1978). For the
employment of visual camouflage, next to the animals size,
structure and colour of the habitat play a major role, as shown for
chameleons (Cuadrado et al., 2001) and moths (Kang et al., 2015).
Orestes mouhotii combines smaller size and stronger crypsis
compared with S. inexpectata, which might be a part of the predator
avoidance strategy of this species. Traction forces, however, were
larger for longer tarsi on some substrates. Higher speed during
locomotion and active escape reactions might be assumed as
potential behavioural traits associated with the longer tarsal length.
Conclusions
This study sheds light on the attachment performance of stick
insects on curved substrates and provides, to the best of our
knowledge, the first quantitative data on traction and pull-off forces
for this group of insects on smooth rods of different diameter. Stick
and leaf insects face several different surface topographies in their
natural habitats, and dominant among these are twigs and branches
of different diameter. The degree of substrate curvature has a
significant influence on the attachment ability of both examined
species, namely higher traction on curved substrates with larger
diameters and higher pull-off force on substrates with lower
diameter. On flat substrates and curved substrates with large
diameters, the two species showed similar traction performance and
much lower pull-off forces than on curved substrates. The traction
force decreases with decreasing stem diameter and the pull-off force
increases with decreasing stem diameter, unless the substrate is
thinner than the tarsal length. On flat substrates and curved
substrates with large diameters, the tarsus length does not
significantly influence the attachment ability. On stems with
diameters lower than the length of the tarsus, the pull-off forces
are reduced, as the contact formation between tarsal attachment pads
and the substrate is reduced. Traction forces, however, are larger for
longer tarsi on stems with a diameter falling below the length of the
tarsus, as the longer tarsi can better clamp onto the substrate between
the contralateral tarsi and produce higher adduction forces, while
shorter tarsi clasp around the stem. The attachment performance is
also dependent on the number of tarsi and tarsomeres in contact,
tarsus position on the tube (e.g. AoA), tarsus and leg orientation, as
well as leg and body configuration on the surface.
Corroborating earlier studies on other insects (e.g. Federle et al.,
2001; Niederegger et al., 2002; Clemente and Federle, 2008), the
pull-off force is dependent on the tibiotarsal angle. On rods, the
pull-off force is higher for higher AoA (or lower tibiotarsal angle).
Furthermore, the AoA probably influences adduction forces,
leading to proper load transmission on the euplantulae, which in
turn influences the traction force. Additionally, the contribution of
claws (Song et al., 2016; Büscher and Gorb, 2019) as well as
differences in the euplantular attachment microstructures present in
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Journal of Experimental Biology
other stick insect species (Büscher et al., 2018a,b, 2019) might also
influence the attachment performance on curved rough substrates.
Surfaces with different degrees of curvature play an important
role for stick insects. Referring to the results of this study, this
induces a much more complex interaction of various phenomena.
The results presented herein further stress the importance of
evaluation of attachment performance on different surface
geometries (Gladun and Gorb 2007; Bußhardt et al., 2014; Voigt
et al., 2017, 2019), besides commonly investigated flat substrates.
Furthermore, insights generated from the present experiments on
curved substrates can be potentially useful for the design of bio-
inspired robotic grippers (e.g. Gorb et al., 2007; Voigt et al., 2012).
Acknowledgements
We thank Chuchu Li and Dennis Petersen (Department of Functional Morphology
and Biomechanics, Kiel University, Germany) for fruitful discussions and Femke
Vogel (same affiliation) for assistance with force measurements. Furthermore, we
thank Holger Dra
̈ger (Schwerin, Germany) and Daniel Dittmar (Berlin, Germany) for
providing the breeding stocks used for the laboratory cultures.
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: T.H.B., S.N.G.; Methodology: T.H.B., S.N.G.; Validation: T.H.B.,
S.N.G.; Formal analysis: T.H.B., M.B.; Investigation: T.H.B., M.B.; Resources:
T.H.B., S.N.G.; Writing - original draft:T.H.B.; Writing - review & editing: T.H.B., M.B.,
S.N.G.; Visualization: T.H.B., M.B.; Supervision: T.H.B., S.N.G.; Project
administration: T.H.B., S.N.G.; Funding acquisition: S.N.G.
Funding
Funding was provided by the Deutsche Forschungsgemeinschaft (grant GO 995/34-1).
Supplementary information
Supplementary information available online at
https://jeb.biologists.org/lookup/doi/10.1242/jeb.226514.supplemental
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RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb226514. doi:10.1242/jeb.226514
Journal of Experimental Biology
Table S1. Measurements of all tarsomeres and the total length of the hind tarsus for Orestes
mouhotii and Sungaya inexpectata (N1,2 = 11).
species
ID
T1 [mm]
T2 [mm]
T3 [mm]
T4 [mm]
T5 [mm]
Lenght
[mm]
Orestes mouhotii
#OM1
1.00
0.47
0.45
0.50
1.06
3.48
Orestes mouhotii
#OM2
0.90
0.42
0.41
0.45
0.95
3.13
Orestes mouhotii
#OM3
1.09
0.51
0.50
0.55
1.16
3.81
Orestes mouhotii
#OM4
0.88
0.41
0.40
0.44
0.93
3.06
Orestes mouhotii
#OM5
1.02
0.48
0.46
0.51
1.08
3.54
Orestes mouhotii
#OM6
0.80
0.37
0.36
0.40
0.85
2.79
Orestes mouhotii
#OM7
1.05
0.49
0.48
0.52
1.11
3.65
Orestes mouhotii
#OM8
1.09
0.51
0.50
0.55
1.16
3.80
Orestes mouhotii
#OM9
1.00
0.47
0.45
0.50
1.06
3.47
Orestes mouhotii
#OM10
0.82
0.38
0.37
0.41
0.87
2.85
Orestes mouhotii
#OM11
0.92
0.43
0.42
0.46
0.98
3.21
Sungaya inexpectata
#SI1
2.91
0.96
0.88
0.92
2.20
7.87
Sungaya inexpectata
#SI2
2.88
0.95
0.88
0.91
2.18
7.80
Sungaya inexpectata
#SI3
2.72
0.90
0.83
0.85
2.05
7.35
Sungaya inexpectata
#SI4
2.98
0.99
0.91
0.94
2.26
8.07
Sungaya inexpectata
#SI5
2.76
0.91
0.84
0.87
2.09
7.46
Sungaya inexpectata
#SI6
2.93
0.97
0.89
0.92
2.22
7.94
Sungaya inexpectata
#SI7
2.90
0.96
0.88
0.91
2.20
7.85
Sungaya inexpectata
#SI8
3.09
1.02
0.94
0.97
2.34
8.35
Sungaya inexpectata
#SI9
2.80
0.93
0.85
0.88
2.12
7.58
Sungaya inexpectata
#SI10
3.16
1.04
0.96
0.99
2.39
8.54
Sungaya inexpectata
#SI11
3.05
1.01
0.93
0.96
2.31
8.26
Journal of Experimental Biology • Supplementary information
Table S2. Measurements of the total length of the tarsi of all three leg pairs for Orestes
mouhotii and Sungaya inexpectata (N1,2 = 15).
Total length [mm]
species
ID
foreleg
midleg
hindleg
Sungaya inexpectata
#SI12
6.6
6.3
7.2
Sungaya inexpectata
#SI13
6.8
6.6
6.7
Sungaya inexpectata
#SI14
6.6
6.8
6.9
Sungaya inexpectata
#SI15
7.0
6.8
7.0
Sungaya inexpectata
#SI16
6.2
6.2
6.2
Sungaya inexpectata
#SI17
6.8
6.7
7.0
Sungaya inexpectata
#SI18
6.8
6.3
6.5
Sungaya inexpectata
#SI19
6.9
6.5
6.8
Sungaya inexpectata
#SI20
6.2
6.7
6.8
Sungaya inexpectata
#SI21
6.3
6.7
6.7
Sungaya inexpectata
#SI22
7.0
6.5
6.9
Sungaya inexpectata
#SI23
7.1
6.8
7.1
Sungaya inexpectata
#SI24
6.8
6.9
6.3
Sungaya inexpectata
#SI25
6.6
6.8
6.4
Sungaya inexpectata
#SI26
6.5
6.7
6.8
Orestes mouhotii
#OM12
3.1
2.8
2.9
Orestes mouhotii
#OM13
3.3
3.7
3.1
Orestes mouhotii
#OM14
3.2
3.8
3.8
Orestes mouhotii
#OM15
3.5
3.5
3.5
Orestes mouhotii
#OM16
2.9
2.9
3.5
Orestes mouhotii
#OM17
3.0
3.2
3.2
Orestes mouhotii
#OM18
3.1
3.5
2.8
Orestes mouhotii
#OM19
3.5
3.7
3.6
Orestes mouhotii
#OM20
2.9
2.9
3.5
Orestes mouhotii
#OM21
3.8
3.0
3.4
Orestes mouhotii
#OM22
3.3
3.0
3.1
Orestes mouhotii
#OM23
3.4
3.4
2.9
Orestes mouhotii
#OM24
3.7
3.2
3.2
Orestes mouhotii
#OM25
3.5
3.3
3.6
Orestes mouhotii
#OM26
3.3
3.4
3.5
Journal of Experimental Biology • Supplementary information
... The force measurement setup ( Figure 3) followed the one used by Büscher and Gorb [26] and Büscher et al. [38] for similar measurements. A BIOPAC Model MP100 and a BIOPAC TCI-102 system (BIOPAC Systems, Inc., Goleta, CA, USA) connected to a force transducer (25 g capacity; FORT25, World Precision Instruments Inc., Sarasota, FL, USA) ...
... The force measurement setup ( Figure 3) followed the one used by Büscher and Gorb [26] and Büscher et al. [38] for similar measurements. A BIOPAC Model MP100 and a BIOPAC TCI-102 system (BIOPAC Systems, Inc., Goleta, CA, USA) connected to a force transducer (25 g capacity; FORT25, World Precision Instruments Inc., Sarasota, FL, USA) were used for the force measurements. ...
... The elevations of the leaves of H. ghiesbreghtii seemed to generate a better holding surface for phasmids. Phasmids already showed an increased pull-off force on curved artificial substrates, if compared to flat surfaces [38]. Similar effects have been observed in other insects [41][42][43][44][45] and frogs [46,47]. ...
Article
Full-text available
Herbivorous insects and plants exemplify a longstanding antagonistic coevolution, resulting in the development of a variety of adaptations on both sides. Some plant surfaces evolved features that negatively influence the performance of the attachment systems of insects, which adapted accordingly as a response. Stick insects (Phasmatodea) have a well-adapted attachment system with paired claws, pretarsal arolium and tarsal euplantulae. We measured the attachment ability of Medauroidea extradentata with smooth surface on the euplantulae and Sungaya inexpectata with nubby microstructures of the euplantulae on different plant substrates, and their pull-off and traction forces were determined. These species represent the two most common euplantulae microstructures, which are also the main difference between their respective attachment systems. The measurements were performed on selected plant leaves with different properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) representing different types among the high diversity of plant surfaces. Wax-crystal-covered substrates with fine roughness revealed the lowest, whereas strongly structured substrates showed the highest attachment ability of the Phasmatodea species studied. Removal of the claws caused lower attachment due to loss of mechanical interlocking. Interestingly, the two species showed significant differences without claws on wax-crystal-covered leaves, where the individuals with nubby euplantulae revealed stronger attachment. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed.
... However, the majority of insects possesses pointed claws with one tip. Research on the claws ranges from experiments on the use and function of species of various taxa, like for example true bugs (Salerno et al. 2018), beetles (Bullock and Federle 2011;Voigt et al. 2019;Salerno et al. 2022), stick insects (Büscher et al. 2020), and flies (Salerno et al. 2020), including locomoting insects, and even their exuviae (Büsse et al. 2019). Furthermore there are investigations on the material properties of the claws (Li et al. 2022). ...
... General attachment capabilities of Sungaya inexpectata on convex substrates of different diameter (Büscher et al. 2020) and synergistic effects between different attachment devices working in concert (Büscher and Gorb 2019) have been previously studied. In this work, we investigated the functional effect of paired claws on attachment performance on four substrates of different roughnesses. ...
... In contrast, in the traction scenario, the animal can extend all its legs into the direction directly opposing the external force pulling parallel to the substrate. This situation makes claws mechanically interlocking and friction force generation possible without any need of force redirection (Büscher et al. 2020). ...
Article
Full-text available
Insect attachment devices and capabilities have been subject to research efforts for decades, and even though during that time considerable progress has been made, numerous questions remain. Different types of attachment devices are known, alongside most of their working principles, however, some details have yet to be understood. For instance, it is not clear why insects for the most part developed pairs of claws, instead of either three or a single one. In this paper, we investigated the gripping forces generated by the stick insect Sungaya inexpectata, in dependence on the number of available claws. The gripping force experiments were carried out on multiple, standardized substrates of known roughness, and conducted in directions both perpendicular and parallel to the substrate. This was repeated two times: first with a single claw being amputated from each of the animals' legs, then with both claws removed, prior to the measurement. The adhesive pads (arolia) and frictional pads (euplantulae) remained intact. It was discovered that the removal of claws had a detractive effect on the gripping forces in both directions, and on all substrates. Notably, this also included the control of smooth surfaces on which the claws were unable to find any asperities to grip on. The results show that there is a direct connection between the adhesive performance of the distal adhesive pad (arolium) and the presence of intact claws. These observations show collective effects between different attachment devices that work in concert during locomotion, and grant insight into why most insects possess two claws.
... females bear an extension in form of a median ridge of the euplantulae on the tarsomeres 2-4 ( Fig. 12B), which is so far not reported for any other phasmid in this form. This accessory ridge can elongate the adhesive surface of the tarsus distally and increase traction along the length of the tarsus, as euplantulae are primarily used for generation of friction in phasmids (Busshardt et al. 2012;Labonte and Federle 2013;Büscher et al. 2020a). However, the arrangement of the euplantulae stabilizes the attachment primarily in the proximal-distal direction, which could be beneficial in the typical postures of these insects in which their legs are arranged circular around the stout body. ...
... However, the arrangement of the euplantulae stabilizes the attachment primarily in the proximal-distal direction, which could be beneficial in the typical postures of these insects in which their legs are arranged circular around the stout body. Furthermore, the elongation of the tarsal chain increases traction on thin stems, if the tarsi grasp around the substrate (Büscher et al. 2020a). A similar effect is additionally achieved by the accessory euplantula on tarsomere 5. ...
Article
Full-text available
With every molecular review involving Chitoniscus Stål, 1875 sensu lato samples from Fiji and New Caledonia revealing polyphyly, the morphology from these two distinct clades was extensively reviewed. Morphological results agree with all previously published molecular studies and therefore Trolicaphyllium gen. nov. is erected to accommodate the former Chitoniscus sensu lato species restricted to New Caledonia, leaving the type species Chitoniscus lobiventris (Blanchard, 1853) and all other Fijian species within Chitoniscus sensu stricto. Erection of this new genus for the New Caledonian species warrants the following new combinations: Trolicaphyllium brachysoma (Sharp, 1898), comb. nov., Trolicaphyllium erosus (Redtenbachher, 1906), comb. nov., and Trolicaphyllium sarrameaense (Größer, 2008a), comb. nov. Morphological details of the female, male, freshly hatched nymph, and egg are illustrated and discussed alongside the Chitoniscus sensu stricto in order to differentiate these two clades which have been mistaken as one for decades.
... The evolution of such egg surface structures and adhesive systems on eggs is likely a similar complex evolutionary scenario, comparable to other aspects of phasmatodean evolution [69,70], such as the tarsal adhesive systems. These also result from complex environmental conditions and are shaped by interactions with various substrates [7,[71][72][73][74][75]. The preferred foodplants that are documented for this insect species are Mangifera indica L. (Anacardiaceae), Nephelium lappaceum L. (Sapindaceae), and Psidium guajava L. (Myrtaceae) and the surface characteristics that are potential adhesive sites are discussed in [15]. ...
Article
Full-text available
Plants and animals are often used as a source for inspiration in biomimetic engineering. However, stronger engagement of biologists is often required in the field of biomimetics. The actual strength of using biological systems as a source of inspiration for human problem solving does not lie in a perfect copy of a single system but in the extraction of core principles from similarly functioning systems that have convergently solved the same problem in their evolution. Adhesive systems are an example of such convergent traits that independently evolved in different organisms. We herein compare two analogous adhesive systems, one from plants seeds and one from insect eggs, to test their properties and functional principles for differences and similarities in order to evaluate the input that can be potentially used for biomimetics. Although strikingly similar, the eggs of the leaf insect Phyllium philippinicum and the seeds of the ivy gourd Coccinia grandis make use of different surface structures for the generation of adhesion. Both employ a water-soluble glue that is spread on the surface via reinforcing fibrous surface structures, but the morphology of these structures is different. In addition to microscopic analysis of the two adhesive systems, we mechanically measured the actual adhesion generated by both systems to quantitatively compare their functional differences on various standardized substrates. We found that seeds can generate much stronger adhesion in some cases but overall provided less reliable adherence in comparison to eggs. Furthermore, eggs performed better regarding repetitive attachment. The similarities of these systems, and their differences resulting from their different purposes and different structural/chemical features, can be informative for engineers working on technical adhesive systems.
... Limb posture also affects attachment forces (Büscher et al. 2020) that are generated by two functionally distinct types of attachment pads on the tarsi (Labonte and Federle 2013) that differentially affect tangential and normal attachment forces of the whole animal (Büscher and Gorb 2019). Posture dependency of attachment forces should also differ between the species used here, owing to different surface structure of tarsal attachment pads (nubby in Carausius and Aretaon, smooth in Medauroidea; Beutel and Gorb 2008;Busshardt et al. 2012). ...
Article
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Overall body proportions and relative limb length are highly characteristic for most insect taxa. In case of the legs, limb length has mostly been discussed with regard to parameters of locomotor performance and, in particular cases, as an adaptation to environmental factors or to the mating system. Here, we compare three species of stick and leaf insects (Phasmatodea) that differ strongly in the length ratio between antennae and walking legs, with the antennae of Medauroidea extradentata being much shorter than its legs, nearly equal length of antennae and legs in Carausius morosus , and considerably longer antennae than front legs in Aretaon asperrimus . We show that that relative limb length is directly related to the near-range exploration effort, with complementary function of the antennae and front legs irrespective of their length ratio. Assuming that these inter-species differences hold for both sexes and all developmental stages, we further explore how relative limb length differs between sexes and how it changes throughout postembryonic development. We show that the pattern of limb-to-body proportions is species-characteristic despite sexual dimorphism, and find that the change in sexual dimorphism is strongest during the last two moults. Finally, we show that antennal growth rate is consistently higher than that of front legs, but differs categorically between the species investigated. Whereas antennal growth rate is constant in Carausius , the antennae grow exponentially in Medauroidea and with a sudden boost during the last moult in Aretaon .
... Smooth attachment pads are found in most groups of insects, for example, in Orthoptera [126][127][128][129][130][131][132][133], Siphonaptera [1], Phthiraptera [1,134], Mantodea [1,135], Hymenoptera [1,[136][137][138][139][140][141][142][143][144][145][146][147][148], Embioptera [109,149,150], Ephemeroptera, in form of a claw pad, [1], Thysanoptera [1,[151][152][153], Blattodea [154][155][156], Phasmatodea [2,59,108,109,[157][158][159][160][161][162][163][164], Stenorrhyncha [66,123,124,165,166], Auchennorrhyncha [167][168][169][170], and some Mecoptera [1,103,171]. ...
Article
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Adhesive pads are functional systems with specific micro- and nanostructures which evolved as a response to specific environmental conditions and therefore exhibit convergent traits. The functional constraints that shape systems for the attachment to a surface are general requirements. Different strategies to solve similar problems often follow similar physical principles, hence, the morphology of attachment devices is affected by physical constraints. This resulted in two main types of attachment devices in animals: hairy and smooth. They differ in morphology and ultrastructure but achieve mechanical adaptation to substrates with different roughness and maximise the actual contact area with them. Species-specific environmental surface conditions resulted in different solutions for the specific ecological surroundings of different animals. As the conditions are similar in discrete environments unrelated to the group of animals, the micro- and nanostructural adaptations of the attachment systems of different animal groups reveal similar mechanisms. Consequently, similar attachment organs evolved in a convergent manner and different attachment solutions can occur within closely related lineages. In this review, we present a summary of the literature on structural and functional principles of attachment pads with a special focus on insects, describe micro- and nanostructures, surface patterns, origin of different pads and their evolution, discuss the material properties (elasticity, viscoelasticity, adhesion, friction) and basic physical forces contributing to adhesion, show the influence of different factors, such as substrate roughness and pad stiffness, on contact forces, and review the chemical composition of pad fluids, which is an important component of an adhesive function. Attachment systems are omnipresent in animals. We show parallel evolution of attachment structures on micro- and nanoscales at different phylogenetic levels, focus on insects as the largest animal group on earth, and subsequently zoom into the attachment pads of the stick and leaf insects (Phasmatodea) to explore convergent evolution of attachment pads at even smaller scales. Since convergent events might be potentially interesting for engineers as a kind of optimal solution by nature, the biomimetic implications of the discussed results are briefly presented.
... Yet, the Heteropterygidae vary significantly in body size, with Dataminae being comparatively small phasmatodeans whereas Heteropteryginae can be impressively large. The tarsal attachment microstructures have been suggested to be partly associated with body size in Heteropterygidae, although the nonuniformity of this trait may be indicative of the occupation of different niches (Büscher et al., 2018a(Büscher et al., , 2018b, 2019) as they reflect adaptations towards different substrate conditions Büscher et al., 2020). Nevertheless, no notable niche differentiation appears to have occurred in Heteropterygidae, the only exception being Heteropteryx whose green, leaf-imitating females and flighted males adapted to a secondary tree-dwelling life style (Bradler & Buckley, 2018). ...
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Stick and leaf insects (Phasmatodea) are large terrestrial herbivorous arthropods known for masquerading as plant parts such as bark, twigs and leaves. Their evolutionary history is largely shaped by convergent evolution associated with adaptive radiations on geographically isolated landmasses that have repeatedly generated ground-dwelling ecomorphs. The members of one lineage, however, the Oriental Heteropterygidae, are morphologically rather uniform, and have a predominantly ground-dwelling lifestyle. The phylogeny of Heteropterygidae that comprises approximately 130 described species is controversial and remains uncertain. In particular, the systematic position of the giant Jungle Nymph Heteropteryx dilatata, whose males are capable of flight and exhibit the most plesiomorphic wing morphology among extant phasmatodeans, is of major interest to the scientific community. Here, we analysed a set of seven nuclear and mitochondrial genes to infer the phylogeny of Heteropterygidae covering the group's overall diversity. The divergence time estimation and reconstruction of the historical biogeography resulted in an ancestral distribution across Sunda-land with long distance dispersal events to Wallacea, the Philippines and the South Pacific. We were able to resolve the relationships among the three principal subgroups of Heteropterygidae and revealed the Dataminae, which contain entirely wingless small forms, as the sister group of Heteropteryginae + Obriminae. Within Heteropteryginae, Haaniella is recovered as paraphyletic in regard to Heteropteryx. Consequently, Heteropteryx must be considered a subordinate taxon deeply embedded within a flightless clade of stick insects. Within Obriminae, the Bornean Hoploclonia is strongly supported as the earliest diverging lineage. Based on this finding, we recognize only two tribes of equal rank among Obriminae, the Hoplocloniini trib. nov. and Obrimini sensu nov. Within the latter, we demonstrate that previous tribal assignments do not reflect phylogenetic relationships and that a basal splitting event occurred between the wing-bearing clade Miroceramia + Pterobrimus and the remaining wingless Obrimini. The Philippine genus Tisamenus is paraphyletic with regard to Ilocano hebardi, thus, we transfer the latter species to Tisamenus as Tisamenus hebardi comb. nov. and synonymize Ilocano with Tisamenus. We discuss character transformations in the light of the new phylogenetic results and conclude that the current taxonomic diversity appears to be mainly driven by allopatry and not to be the result of niche differentiation. This radiation is thus best described as a nonadaptive radiation.
... The detachment force was measured by pulling the test surface away from the sensor at an angle of 90° and with a speed of ~1-2 cm/s using a laboratory lifting platform. The highest peak of the obtained graph was considered the maximum detachment force (see in [22,78,79]). All experiments were performed at 20-22 °C temperature and 40-60% relative humidity. ...
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Leaf insects (Phylliidae) are well-camouflaged terrestrial herbivores. They imitate leaves of plants almost perfectly and even their eggs resemble seeds—visually and regarding to dispersal mechanisms. The eggs of the leaf insect Phyllium philippinicum utilize an adhesive system with a combination of glue, which can be reversibly activated through water contact and a water-responding framework of reinforcing fibers that facilitates their adjustment to substrate asperities and real contact area enhancement. So far, the chemical composition of this glue remains unknown. To evaluate functional aspects of the glue–solvent interaction, we tested the effects of a broad array of chemical solvents on the glue activation and measured corresponding adhesive forces. Based on these experiments, our results let us assume a proteinaceous nature of the glue with different functional chemical subunits, which enable bonding of the glue to both the surface of the egg and the unpredictable substrate. Some chemicals inhibited adhesion, but the deactivation was always reversible by water-contact and in some cases yielded even higher adhesive forces. The combination of glue and fibers also enables retaining the adhesive on the egg, even if detached from the egg’s surface. The gained insights into this versatile bioadhesive system could hereafter inspire further biomimetic adhesives.
Article
Background: Lepidoptera is the largest order of insects, some of which are major pests of crops and forests. The cuticles of lepidopteran pests play important roles in defense against insecticides and pathogens, and are indispensable for constructing and maintaining extracellular structures and locomotion during their life cycle. Lepidopteran-specific cuticular proteins could be potential targets for lepidopteran pest control. But information on this is limited. Our research aimed to screen the lepidopteran-specific cuticular proteins using the lepidopteran model, the silkworm, to explore the molecular mechanism underlying the involvement of cuticular proteins in body shape construction. Results: Positional cloning showed that BmLSPMP-like, a gene encoding a lepidopteran-specific peritrophic matrix protein (PMP) like protein which includes a peritrophin A-type chitin-binding domain (CBM_14), is responsible for the stick (sk) mutation. BmLSPMP-like is an evolutionarily conserved gene that exhibits synteny in Lepidoptera and underwent purifying selection during evolution. Expression profiles demonstrated that BmLSPMP-like is expressed in chitin-forming tissues, testis and ovary, and accumulates in the cuticle. BmLSPMP-like knockout, generated with CRISPR/Cas9, resulted in a stick-like larval body shape phenotype. Over-expression of BmLSPMP-like in the sk mutant rescued its abnormal body shape. The results showed that BmLSPMP-like may be involved in assemblage in the larval cuticle. Conclusion: Our results suggested that the dysfunction of BmLSPMP-like may result in a stick body shape phenotype in silkworm, through the regulation of the arrangement of the chitinous laminae and cuticle thickness. Our study provides new evidence of the effects of LSPMP-likes on lepidopteran body shape formation, metamorphosis and mortality, which could be an eco-friendly target for lepidopteran pest management. This article is protected by copyright. All rights reserved.
Article
Most insects can regulate friction with their seta structure when moving or crawling. To investigate the complicated friction behavior brought by the large deflection of seta structure, the nonlinear cantilever beam model with reactive support and friction force was established. The friction experiments of the seta structure were also conducted to verify the analytical results. The effect of loading conditions on the friction behavior of seta structure was discussed. It demonstrates that the friction force reacts nonlinearly with the applied normal displacement and exhibits obvious friction-reduction. The seta structure exhibits frictional anisotropy when sliding forward or backward which becomes more pronounced for small applied displacement and initial angle. Those findings provide valuable insights into the insects’ tribology mechanisms.
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The attachment function of tibial spurs and pretarsal claws in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae) during locomotion was examined in this study. First, we measured the angle, at which the beetles detached from substrates with different roughness. At a surface roughness of 12 μm and higher, intact animals were able to cling to a completely tilted platform (180°). Second, we estimated the forces the beetles could exert in walking on smooth and rough cylinders of different diameters, on a plane and also between two plates. To elucidate the role of the individual structures, we ablated them consecutively. We found tibial spurs not to be in use in walking on flat substrates. On some of the curved substrates, ablation of tibial spurs caused an effect. A clear effect of tibial spurs was revealed in walking between two plates. Thus, these structures are probably used for generating propulsion in narrowed spaces.
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Stick and leaf insects (Phasmatodea) are large, tropical, predominantly nocturnal herbivores, which exhibit extreme masquerade crypsis, whereby they morphologically and behaviorally resemble twigs, bark, lichen, moss, and leaves. Females employ a wide range of egg-laying techniques, largely corresponding to their ecological niche, including dropping or flicking eggs to the forest floor, gluing eggs to plant substrate, skewering eggs through leaves, ovipositing directly into the soil, or even producing a complex ootheca. Phasmids are the only insects with highly species-specific egg morphology across the entire order, with specific egg forms that correspond to oviposition technique. We investigate the temporal, biogeographic, and phylogenetic pattern of evolution of egg-laying strategies in Phasmatodea. Our results unequivocally demonstrate that the ancestral oviposition strategy for female stick and leaf insects is to remain in the foliage and drop or flick eggs to the ground, a strategy that maintains their masquerade. Other major key innovations in the evolution of Phasmatodea include the (1) hardening of the egg capsule in Euphasmatodea; (2) the repeated evolution of capitulate eggs (which induce ant-mediated dispersal, or myrmecochory); (3) adapting to a ground or bark dwelling microhabitat with a corresponding shift in adult and egg phenotype and egg deposition directly into the soil; and (4) adhesion of eggs in a clade of Necrosciinae that led to subsequent diversification in oviposition modes and egg types. We infer at minimum 16 independent origins of a burying/inserting eggs into soil/crevices oviposition strategy, 7 origins of gluing eggs to substrate, and a single origin each of skewering eggs through leaves and producing an ootheca. We additionally discuss the systematic implications of our phylogenetic results. Aschiphasmatinae is strongly supported as the earliest diverging extant lineage of Euphasmatodea. Phylliinae and Diapheromerinae are both relatively early diverging euphasmatodean taxa. We formally transfer Otocrania from Cladomorphinae to Diapheromerinae and recognize only two tribes within Diapheromerinae: Diapheromerini sensu nov. and Oreophoetini sensu nov. We formally recognize the clade comprising Necrosciinae and Lonchodinae as Lonchodidae stat. rev. sensu nov.
Article
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Prehensile and gripping organs are recurring structures in different organisms that enhance friction by the reinforcement and redirection of normal forces. The relationship between organ structure and biomechanical performance is poorly understood, despite a broad relevance for microhabitat choice, movement ecology and biomimetics. Here, we present the first study of the biomechanics of prehensile feet in long-legged harvestmen. These arachnids exhibit the strongest sub-division of legs among arthropods, permitting extreme hyperflexion (i.e. curling up the foot tip). We found that despite the lack of adhesive foot pads, these moderately sized arthropods are able to scale vertical smooth surfaces, if the surface is curved. Comparison of three species of harvestmen differing in leg morphology shows that traction reinforcement by foot wrapping depends on the degree of leg sub-division, not leg length. Differences are explained by adaptation to different microhabitats on trees. The exponential increase of foot section length from distal to proximal introduces a gradient of flexibility that permits adaptation to a wide range of surface curvature while maintaining integrity at strong flexion. A pulley system of the claw depressor tendon ensures the controlled flexion of the high number of adesmatic joints in the harvestman foot. These results contribute to the general understanding of foot function in arthropods and showcase an interesting model for the biomimetic engineering of novel transportation systems and surgical probes.
Chapter
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Stick and leaf insects (order Phasmatodea) are a mesodiverse lineage of large terrestrial herbivores with predominantly tropical distribution and few species inhabiting more temperate regions. The phylogenetic position of the Phasmatodea among the lower neopteran insects has been debated for many years, with basically every orthopteroid insect order proposed as the potential sister taxon. The stick and leaf insects exhibit a remarkably poor fossil record. The fascinating and variable biology of stick insects has made them excellent model systems for investigating a number of evolutionary phenomena, including speciation and reproductive isolation, evolution of parthenogenesis and alternative reproductive strategies, and more recently the evolution of cold tolerance. Evidence for monophyletic Phasmatodea is undisputed and has grown stronger in recent years, with evidence coming from various sources. The chapter lists and discusses the currently recognized, non‐encaptic monophyletic groups. The contributions of amateur taxonomists play a crucial role in describing the phasmatodean diversity.
Research
http://phasmida.speciesfile.org The Phasmida Species File (PSF) is a taxonomic database of the world's Phasmida (stick and leaf insects, known as walking sticks and walking leaves in the U.S.). There is full synonymic and taxonomic information for 3,350 valid species and 5,300 taxonomic names, 37,500 citations to 3,178 references, over 7,600 specimen records and 16,800 images of 75% of valid species, with more being added to on a regular basis. Another future aim of this database is to provide high quality images of living phasmids in the wild. The PSF is annually in fed into the catalogue of life (Species 2000: Naturalis, Leiden, the Netherlands).
Article
Stick insects are well adapted in their locomotion to various surfaces and topographies of natural substrates. Single pad measurements characterised the pretarsal arolia of these insects as shear-sensitive adhesive pads and the tarsal euplantulae as load-sensitive friction pads. Different attachment microstructures on the euplantulae reveal an adaptation of smooth euplantulae to smooth surfaces and nubby eupantulae to a broader range of surface roughnesses. How different attachment pads and claws work in concert, and how strong the contribution of different structures to the overall attachment performance is, however, remains unclear. We therefore assessed combinatory effects in the attachment system of two stick insect species with different types of euplantular microstructures by analysing their usage in various posture situations and the performance on different levels of substrate roughness. For comparison, we provide attachment force data of the whole attachment system. The combination of claws, arolia and euplantulae provides mechanical interlocking on rough surfaces, adhesion and friction on smooth surfaces in different directions and facilitates attachment on different inclines and on a broad range of surface roughnesses, with the least performance in a range of 0.3 - 1.0 µm. On smooth surfaces stick insects use arolia always, but employ euplantulae, if the body weight can generate load on them (upright, wall). On structured surfaces, claws enable mechanical interlocking at roughnesses higher than 12 µm. On less structured surfaces, the attachment strength depends on the use of pads and, corroborating earlier studies, favours smooth pads on smooth surfaces, but nubby euplantulae on micro-rough surfaces.
Article
The ability to climb with adhesive pads conveys significant advantages and is widespread in the animal kingdom. The physics of adhesion predict that attachment is more challenging for large animals, whereas detachment is harder for small animals, due to the difference in surface-to-volume ratios. Here, we use stick insects to show that this problem is solved at both ends of the scale by linking adhesion to the applied shear force. Adhesive forces of individual insect pads, measured with perpendicular pull-offs, increased approximately in proportion to a linear pad dimension across instars. In sharp contrast, whole-body force measurements suggested area scaling of adhesion. This discrepancy is explained by the presence of shear forces during whole-body measurements, as confirmed in experiments with pads sheared prior to detachment. When we applied shear forces proportional to either pad area or body weight, pad adhesion also scaled approximately with area or mass, respectively, providing a mechanism that can compensate for the size-related loss of adhesive performance predicted by isometry. We demonstrate that the adhesion-enhancing effect of shear forces is linked to pad sliding, which increased the maximum adhesive force per area sustainable by the pads. As shear forces in natural conditions are expected to scale with mass, sliding is more frequent and extensive in large animals, thus ensuring that large animals can attach safely, while small animals can still detach their pads effortlessly. Our results therefore help to explain how nature's climbers maintain a dynamic attachment performance across seven orders of magnitude in body weight.
Article
Published in Zoologica — Original Contributions to Zoology (ISSN 0044-5088): Abstract Attachment devices with different microstructure and surface microstructure evolved on the tarsi of hexapods. In biomechanical studies it was shown for a few species that different types of structure have different attachment properties. However, it is yet unclear if these structures evolved in correlation with the species’ ecology. Stick and leaf insects (Phasmatodea) is a speciose insect taxon with several different ecological preferences. We therefore chose 116 species from all subfamilies currently recognised within this taxon, to uncover correlations between the euplantular microstructure and the ecological preferences or oviposition techniques of the examined species. Twelve different types of attachment microstructures have been found using scanning electron microscopy (SEM), seven of them previously unknown. The correlation of the microstructures with the ecology, habitat and phylogeny of stick and leaf insects is discussed. Two different hypotheses are possible based on this analysis: (1) Smooth euplantular structures may be a ground plan in Phasmatodea and structures with different degrees of elevations evolved convergently in many groups starting from this type of microstructures, or (2) elongated acanthae are the plesiomorphic state which is conserved in some taxa and convergently reduced to smooth types of microstructures in other groups. These assumptions should be tested in subsequent phylogenetic studies based on the use of extensive molecular data. In addition, one species of Embioptera (Hexapoda), which is assumed to be the sister group of the Phasmatodea, has been examined, and its rather smooth attachment structures might be a result of their extraordinary mode of living within galleries. URL: https://www.schweizerbart.de/publications/detail/isbn/9783510550517/Zoologica_Vol_164
Chapter
Specific mechanisms of adhesion found in nature are discussed in the previous chapter (|Chap. 54, "Bioadhesives"). One of the most discussed biological systems in the last decade are the so-called fibrillar adhesives of insects, spiders, and geckos. These systems are adapted for dynamic adhesion of animals during locomotion and, therefore, have some extraordinary properties, such as (1) directionality, (2) preload by shear, (3) quick detachment by peeling, (4) low dependence on the substrate chemistry, (5) reduced ability to contamination and selfcleaning, and (6) the absence or strong reduction of self-adhesion. In the present chapter, we review functional principles of such biological systems in various animal groups with an emphasis on insects and discuss their biomimetic potential. The data on ultrastructure and mechanics of materials of adhesive pads, movements during contact formation and breakage, the role of the fluid in the contact between the pad and substrate are presented here. The main goal is to demonstrate how a comparative experimental approach in studies of biological systems aids in the development of novel adhesive materials and systems. The microstructured adhesive systems, inspired by studies of biological systems of insects, spiders, and geckos, are also shortly reviewed. © Springer International Publishing AG, part of Springer Nature 2018. All rights are reserved.